Christel Uittenbogaart, MD

Affiliations
Director, Immuno/BioSpot Core

Professor, Pediatrics, Microbiology, Immunology & Molecular Genetics

Member, Cell & Developmental Biology GPB Home Area,Immunity, Microbes &
 

Molecular Pathogenesis GPB Home Area, Tumor Immunology Program at the Jonsson Comprehensive Cancer Center (JCCC)

Research Interests
Human T cell development is the major focus of the laboratory. The thymus is the central organ where T cell receptor (TCR) alpha/beta cells as well as other rare hematopoietic cell types develop from intrathymic stem cells. These cell types include TCR gamma/delta cells, plasmacytoid (lymphoid -derived) dendritic cells, myeloid derived dendritic cells, Natural Killer (NK) cells, NK-T cells and regulatory T cells. These rare cell populations comprise potent immunoregulatory cells that link the innate and adaptive immune response as they carry out their function in the periphery against various pathogens such as human immunodeficiency virus (HIV). HIV actively replicates in the human thymus and disrupts normal T cell development contributing to the overall immune dysfunction seen in HIV infected individuals. This is particularly obvious during fetal and postnatal life when the thymus is most active. The focus of our laboratory is to; 1) elucidate factors such as chemokines and cytokines involved in thymopoiesis that can be exploited to boost T cell developmental processes; 2) investigate the function of intrathymic dendritic cells such as plasmacytoid dendritic cells, the natural Interferon-alpha (IFN-alpha) producing cells, and myeloid dendritic cells in normal T cell development; 3) evaluate the mechanism of the immunosuppressive effects of high levels of IFN-alpha observed in certain diseases; 4) examine the cytopathicity, replicative capacity, and cell tropism of various pediatric HIV isolates in the thymus; 5) determine the role of regulatory T cells in thymic HIV infection. We utilize three different model systems to study T cell development: in vitro thymocyte suspension culture, thymus organ culture, and human thymus grafts in the SCID-hu mouse. The goal of our research is to gain a better understanding of the development and function of the immune system in order to facilitate the development and design of novel therapeutic approaches to immunodeficiency such as observed after chemotherapy, bone marrow transplantation and in HIV disease.

Biography
Human T Cell Development Studies of human T cell development are the major focus of the laboratory. These studies are being pursued in in vitro thymocyte suspension cultures, thymic organ culture and in vivo in the SCID/hu mouse. We are interested in examining the role of cytokines on normal thymocyte maturation. We want to assess whether cytokine administration can augment stem cell reconstitution strategies in diseases such as infection with the human immunodeficiency virus (HIV) and malignancies. In addition, understanding the interaction between HIV and the developing T cell in the thymus is an important focus of the laboratory. Our studies are intended to test the hypotheses that; 1). thymocyte subsets which are activated and/or proliferating are the principle targets for HIV infection; 2). cytopathic viral strains affect thymocytes at an earlier stage of maturation than non-cytopathic strains and; 3). depletion of thymocytes which produce IFN-g results in increased HIV expression by thymocytes and contributes to immunodeficiency. Studies of human T cell development are the major focus of the laboratory. These studies are being pursued are in vitro thymocyte suspension cultures, thymic organ cultures and in vivo in the SCID/hu mouse. We are interested in examining the role of cytokines on normal thymocyte maturation. We want to assess whether cytokine administration can augment stem cell reconstitution strategies in disease such as infection with the human immunodeficiency virus (HIV) and malignancies. In addition, understanding the interaction between HIV and the developing T cell in the thymus is an important focus of the laboratory. Our studies are intended to test the hypothesis that; 1) thymocyte subsets which are activated and/or proliferating are the targets for HIV infection; 2) cytopathic viral strains affect thymocytes at an earlier stage of maturation than non-cytopathic strains and; 3) depletion of thymocytes which produce IFN-. results in increased HIV expression by thymocytes and contribution to immunodeficiency. Besides studying the effects of HIV on the developing immune system, we are continuing our research to determine how cytokines affect cell growth and the phenotype of malignant immature T cell leukemias. We have shown that there is a correlation between stage of maturation of the T cell leukemias and expression of the transcription factor c-jun which binds to the AP-1 binding site. Therefore, we want to delineate the role of the nuclear factors in normal and malignant T cell growth and differentiation. Understanding the normal developing immune system and its deregulation in HIV disease and leukemias may provide new avenues for medical intervention.

Publications

Legrand Nicolas, van der Velden Gisela J, Ho Tsong Fang Raphael, Douaisi Marc, Weijer Kees, Das Atze T, Blom Bianca, Uittenbogaart Christel H, Berkhout Ben, Centlivre Mireille A doxycycline-dependent HIV-1 replicates in vivo without inducing CD4+ T-cell depletion. The Journal of general virology. 2012; .

Colantonio Arnaud D, Epeldegui Marta, Jesiak Maria, Jachimowski Loes, Blom Bianca, Uittenbogaart Christel H IFN-α is constitutively expressed in the human thymus, but not in peripheral lymphoid organs. PloS one. 2011; 6(8): e24252.

Halnon Nancy J, Cooper Paige, Chen Diana Yu Hui, Boechat M Ines, Uittenbogaart Christel H Immune dysregulation after cardiothoracic surgery and incidental thymectomy: maintenance of regulatory T cells despite impaired thymopoiesis. Clinical & developmental immunology. 2011; 2011: 915864.

Truong Hong-Ha M, Sim Myung S, Dillon Maryanne, Uittenbogaart Christel H, Dickover Ruth, Plaeger Susan F, Bryson Yvonne J Correlation of immune activation during late pregnancy and early postpartum with increases in plasma HIV RNA, CD4/CD8 T cells, and serum activation markers. Clinical and vaccine immunology : CVI. 2010; 17(12): 2024-8.

Schotte Remko, Schmidlin Heike, Nagasawa Maho, Dontje Wendy, Karrich Julien J, Uittenbogaart Christel, Spits Hergen, Blom Bianca Isolation and in vitro generation of gene-manipulated human plasmacytoid and conventional dendritic cells. Methods in molecular biology (Clifton, N.J.). 2010; 595(5): 67-85.

Furler Robert L, Uittenbogaart Christel H Signaling through the P38 and ERK pathways: a common link between HIV replication and the immune response. Immunologic research. 2010; 48(1-3): 99-109.

Hwang Seungmin, Wu Ting-Ting, Tong Leming M, Kim Kyeong Seon, Martinez-Guzman DeeAnn, Colantonio Arnaud D, Uittenbogaart Christel H, Sun Ren Persistent gammaherpesvirus replication and dynamic interaction with the host in vivo. Journal of virology. 2008; 82(24): 12498-509.

Schmidlin Heike, Diehl Sean A, Nagasawa Maho, Scheeren Ferenc A, Schotte Remko, Uittenbogaart Christel H, Spits Hergen, Blom Bianca Spi-B inhibits human plasma cell differentiation by repressing BLIMP1 and XBP-1 expression. Blood. 2008; 112(5): 1804-12.

Ho Tsong Fang Raphael, Colantonio Arnaud D, Uittenbogaart Christel H The role of the thymus in HIV infection: a 10 year perspective. AIDS (London, England). 2008; 22(2): 171-84.

Schmid Ingrid, Uittenbogaart Christel, Jamieson Beth D Live-cell assay for detection of apoptosis by dual-laser flow cytometry using Hoechst 33342 and 7-amino-actinomycin D. Nature protocols. 2007; 2(1): 187-90.

An Dong Sung, Poon Betty, Ho Tsong Fang Raphael, Weijer Kees, Blom Bianca, Spits Hergen, Chen Irvin S Y, Uittenbogaart Christel H Use of a novel chimeric mouse model with a functionally active human immune system to study human immunodeficiency virus type 1 infection.Clinical and vaccine immunology : CVI. 2007; 14(4): 391-6.

Ho Tsong Fang, R. Uittenbogaart, C. H. Hurtrel, B. HIV and the hidden face of the thymus. Aids. 2006; 20(17): 2240-2242.

Gurney, K. B. Uittenbogaart, C. H. Human immunodeficiency virus persistence and production in T-cell development. Clin Vaccine Immunol. 2006; 13(11): 1237-45.

Pedroza-Martins, L. Boscardin, W. J. Anisman-Posner, D. J. Redsar, B. N. Bryson, Y. J. Yang, O. O. Uittenbogaart, C. H. Interferon-gamma decreases replication of primary R5 HIV-1 isolates in thymocytes. Aids. 2006; 20(6): 939-42.

Schmidlin, H. Dontje, W. Groot, F. Ligthart, S. J. Colantonio, A. D. Oud, M. E. Schilder-Tol, E. J. Spaargaren, M. Spits, H. Uittenbogaart, C. H. Blom, B. Stimulated plasmacytoid dendritic cells impair human T-cell development. Blood. 2006; 108(12): 3792-800.

Yang, O. O. Lin, H. Dagarag, M. Ng, H. L. Effros, R. B. Uittenbogaart, C. H. Decreased perforin and granzyme B expression in senescent HIV-1-specific cytotoxic T lymphocytes. Virology. 2005; 332(1): 16-9.

Lubong, R. Ng, H. L. Uittenbogaart, C. H. Yang, O. O. Culturing of HIV-1-specific cytotoxic T lymphocytes with interleukin-7 and interleukin-15. Virology. 2004; 325(2): 175-80.

Gurney, K. B. Colantonio, A. D. Blom, B. Spits, H. Uittenbogaart, C. H. Endogenous IFN-alpha production by plasmacytoid dendritic cells exerts an antiviral effect on thymic HIV-1 infection. J Immunol. 2004; 173(12): 7269-76.

Gimeno, R. Weijer, K. Voordouw, A. Uittenbogaart, C. H. Legrand, N. Alves, N. L. Wijnands, E. Blom, B. Spits, H. Monitoring the effect of gene silencing by RNA interference in human CD34+ cells injected into newborn RAG2-/- gammac-/- mice: functional inactivation of p53 in developing T cells. Blood. 2004; 104(13): 3886-93.

Wilson, C. B. Uittenbogaart, C. H. Mathis, D. J. Immunology at Asilomar: from molecules to mice. Nat Immunol. 2003; 4(4): 300-2.

Sprent, J. Uittenbogaart, C. H. Fink, P. J. A season for midwinter immunology. Nat Immunol. 2002; 3(5): 414-6.

Pedroza-Martins, L. Boscardin, W. J. Anisman-Posner, D. J. Schols, D. Bryson, Y. J. Uittenbogaart, C. H. Impact of cytokines on replication in the thymus of primary human immunodeficiency virus type 1 isolates from infants. J Virol. 2002; 76(14): 6929-43.

Weijer, K. Uittenbogaart, C. H. Voordouw, A. Couwenberg, F. Seppen, J. Blom, B. Vyth-Dreese, F. A. Spits, H. Intrathymic and extrathymic development of human plasmacytoid dendritic cell precursors in vivo. Blood. 2002; 99(8): 2752-9.

Gurney, K. B. Yang, O. O. Wilson, S. B. Uittenbogaart, C. H. TCR gamma delta+ and CD161+ thymocytes express HIV-1 in the SCID-hu mouse, potentially contributing to immune dysfunction in HIV infection. J Immunol. 2002; 169(9): 5338-46.

Schmid, I. Hausner, M. A. Cole, S. W. Uittenbogaart, C. H. Giorgi, J. V. Jamieson, B. D. Simultaneous flow cytometric measurement of viability and lymphocyte subset proliferation. J Immunol Methods. 2001; 247(1-2): 175-86.

Uittenbogaart, C. H. Boscardin, W. J. Anisman-Posner, D. J. Koka, P. S. Bristol, G. Zack, J. A. Effect of cytokines on HIV-induced depletion of thymocytes in vivo. Aids. 2000; 14(10): 1317-25.

Spits, H. Couwenberg, F. Bakker, A. Q. Weijer, K. Uittenbogaart, C. H. Id2 and Id3 inhibit development of CD34(+) stem cells into predendritic cell (pre-DC)2 but not into pre-DC1. Evidence for a lymphoid origin of pre-DC2. J Exp Med. 2000; 192(12): 1775-84.

Schmid, I. Ferbas, J. Uittenbogaart, C. H. Giorgi, J. V. Flow cytometric analysis of live cell proliferation and phenotype in populations with low viability. Cytometry. 1999; 35(1): 64-74.

Krogstad, P. Uittenbogaart, C. H. Dickover, R. Bryson, Y. J. Plaeger, S. Garfinkel, A. Primary HIV infection of infants: the effects of somatic growth on lymphocyte and virus dynamics. Clin Immunol. 1999; 92(1): 25-33.

Economides, A. Schmid, I. Anisman-Posner, D. J. Plaeger, S. Bryson, Y. J. Uittenbogaart, C. H. Apoptosis in cord blood T lymphocytes from infants of human immunodeficiency virus-infected mothers. Clin Diagn Lab Immunol. 1998; 5(2): 230-4.

Pedroza-Martins, L. Gurney, K. B. Torbett, B. E. Uittenbogaart, C. H. Differential tropism and replication kinetics of human immunodeficiency virus type 1 isolates in thymocytes: coreceptor expression allows viral entry, but productive infection of distinct subsets is determined at the postentry level. J Virol. 1998; 72(12): 9441-52.

Uittenbogaart, C. H. Law, W. Leenen, P. J. Bristol, G. van Ewijk, W. Hays, E. F. Thymic dendritic cells are primary targets for the oncogenic virus SL3-3. J Virol. 1998; 72(12): 10118-25.

Perillo, N. L. Uittenbogaart, C. H. Nguyen, J. T. Baum, L. G. Galectin-1, an endogenous lectin produced by thymic epithelial cells, induces apoptosis of human thymocytes. J Exp Med. 1997; 185(10): 1851-8.

Jamieson, B. D. Uittenbogaart, C. H. Schmid, I. Zack, J. A. High viral burden and rapid CD4+ cell depletion in human immunodeficiency virus type 1-infected SCID-hu mice suggest direct viral killing of thymocytes in vivo. J Virol. 1997; 71(11): 8245-53.

Kitchen, S. G. Uittenbogaart, C. H. Zack, J. A. Mechanism of human immunodeficiency virus type 1 localization in CD4-negative thymocytes: differentiation from a CD4-positive precursor allows productive infection. J Virol. 1997; 71(8): 5713-22.

Baum, L. G. Derbin, K. Perillo, N. L. Wu, T. Pang, M. Uittenbogaart, C. Characterization of terminal sialic acid linkages on human thymocytes. Correlation between lectin-binding phenotype and sialyltransferase expression.J Biol Chem. 1996; 271(18): 10793-9.

Uittenbogaart, C. H. Anisman, D. J. Jamieson, B. D. Kitchen, S. Schmid, I. Zack, J. A. Hays, E. F. Differential tropism of HIV-1 isolates for distinct thymocyte subsets in vitro. Aids. 1996; 10(7): F9-16.

Uittenbogaart, C. H. Schmidc, I. Kiertscher, S. Shau, H. Anisman, D. J. Zsebo, K. M. Clement, L. T. Human thymocyte responsiveness to stem cell factor: synergy with interleukin-2 for the generation of NK/LAK cytotoxicity.Immunol Lett. 1996; 52(1): 45-52.

Uittenbogaart,C.H. Anisman,D.J. Zack,J.A. Economides,A. Schmid,I. Hays,E.F. Effects of cytokines on HIV-1 production by thymocytes. Thymus 1995; 23: 155-175.

Baum, L. G. Pang, M. Perillo, N. L. Wu, T. Delegeane, A. Uittenbogaart, C. H. Fukuda, M. Seilhamer, J. J. Human thymic epithelial cells express an endogenous lectin, galectin-1, which binds to core 2 O-glycans on thymocytes and T lymphoblastoid cells. J Exp Med. 1995; 181(3): 877-87.

Mitrovic, B. Ignarro, L. J. Vinters, H. V. Akers, M. A. Schmid, I. Uittenbogaart, C. Merrill, J. E. Nitric oxide induces necrotic but not apoptotic cell death in oligodendrocytes. Neuroscience. 1995; 65(2): 531-9.

Schmid, I. Uittenbogaart, C. H. Keld, B. Giorgi, J. V. A rapid method for measuring apoptosis and dual-color immunofluorescence by single laser flow cytometry. J Immunol Methods. 1994; 170(2): 145-57.

Uittenbogaart, C. H. Anisman, D. J. Zack, J. A. Economides, A. Schmid, I. Hays, E. F. Effects of cytokines on HIV-1 production by thymocytes. Thymus. 1994; 23(3-4): 155-75.

Schmid, I. Uittenbogaart, C. H. Giorgi, J. V. Sensitive method for measuring apoptosis and cell surface phenotype in human thymocytes by flow cytometry.Cytometry. 1994; 15(1): 12-20.

Uittenbogaart, C. H. Anisman, D. J. Tary-Lehmann, M. Vollger, L. W. Breit, T. M. Van Dongen, J. J. Saxon, A. The SCID mouse environment causes immunophenotypic changes in human immature T-cell lines. Int J Cancer. 1994; 56(4): 546-51.

Uittenbogaart,C.H. Anisman,D.J. Tary-Lehmann,M. Vollger,L.W. Saxon,A. The SCID mouse: an in-vivo model to study human immature T cell leukemias. Int.J.Cancer 1994; 56: 546-551.

Vollger, L. W. Uittenbogaart, C. H. Interleukin-7 promotes the generation of phenotypically mature CD45RA positive human thymocytes in vitro. Cytokine. 1993; 5(2): 157-68.

Genot, E. M. Meier, K. E. Licciardi, K. A. Ahn, N. G. Uittenbogaart, C. H. Wietzerbin, J. Clark, E. A. Valentine, M. A. Phosphorylation of CD20 in cells from a hairy cell leukemia cell line. Evidence for involvement of calcium/calmodulin-dependent protein kinase II. J Immunol. 1993; 151(1): 71-82.

Genot,E. Meier,K.E. Licciardi,K.A. Uittenbogaart,C.H. Wietzerbin,J. Clark,E.A. Valentine,M.A. Phosphorylation of the CD20 phosphoprotein in a hairy cell leukemic line. J.Immunol 1993; 151: 71-82.

Schmid, I. Krall, W. J. Uittenbogaart, C. H. Braun, J. Giorgi, J. V. Dead cell discrimination with 7-amino-actinomycin D in combination with dual color immunofluorescence in single laser flow cytometry.Cytometry. 1992; 13(2): 204-8.

Hays, E. F. Uittenbogaart, C. H. Brewer, J. C. Vollger, L. W. Zack, J. A. In vitro studies of HIV-1 expression in thymocytes from infants and children. Aids. 1992; 6(3): 265-72.

Schmid, I. Uittenbogaart, C. H. Giorgi, J. V. A gentle fixation and permeabilization method for combined cell surface and intracellular staining with improved precision in DNA quantification. Cytometry. 1991; 12(3): 279-85.

Uittenbogaart, C. H. Higashitani, S. Schmid, I. Vollger, L. W. Boone, T. Clement, L. T. Interleukin-4 induces expression of the CD45RA antigen on human thymocyte subpopulations. Int Immunol. 1990; 2(12): 1179-87.

Ueno, Y. Hays, E. F. Hultin, L. Uittenbogaart, C. H. Human thymocytes do not respond to interleukin-2 after removal of mature “bright” CD5 positive cells. Cell Immunol. 1989; 124(2): 239-51.

Ueno, Y. Boone, T. Uittenbogaart, C. H. Selective stimulation of human thymocyte subpopulations by recombinant IL-4 and IL-3. Cell Immunol. 1989; 118(2): 382-93.
Nishanian, P. G. Ojo-Amaize, E. Uittenbogaart, C. H. Giorgi, J. V. A simple and rapid method for preparation of HIV-expressing targets for functional assays. J Immunol Methods. 1988; 107(2): 261-71.

Hays, E. F. Kitada, S. Uittenbogaart, C. H. Reeve, J. R., Jr. Autocrine growth of murine lymphoma cells. J Natl Cancer Inst. 1988; 80(2): 116-21.
Kanowith-Klein, S. Saxon, A. Uittenbogaart, C. H. Constitutive production of B cell differentiation factor-like activity by human T and B cell lines. Eur J Immunol. 1987; 17(5): 593-8.

Uittenbogaart, C. H. Nishanian, P. G. Anisman, D. J. Erikson, T. K. Fahey, J. L. Leukemia derived growth factors produced by human malignant T-lymphoid cell lines.Cancer Res. 1986; 46(3): 1219-23.
Kermani-Arab, V. Uittenbogaart, C. Bramhall, J. Purification of human interleukin 2 produced from normal human peripheral blood mononuclear cells. Thymus. 1986; 8(1-2): 3-11.

Uittenbogaart, C. H. Fahey, J. L. Leukemia derived growth factors. Lymphokine Res. 1984; 3(2): 39-44.

Hays, E. F. Goodrum, D. Bessho, M. Kitada, S. Uittenbogaart, C. H. Leukemia-derived growth factor (non-interleukin-2) produced by murine lymphoma T-cell lines.Proc Natl Acad Sci U S A. 1984; 81(24): 7807-11.

Merrill, J. E. Mohlstrom, C. Uittenbogaart, C. Kermaniarab, V. Ellison, G. W. Myers, L. W. Response to and production of interleukin 2 by peripheral blood and cerebrospinal fluid lymphocytes of patients with multiple sclerosis. J Immunol. 1984; 133(4): 1931-7.

Uittenbogaart, C. H. Cantor, Y. Fahey, J. L. Growth of human malignant lymphoid cell lines in serum-free medium. In Vitro. 1983; 19(1): 67-72.

Uittenbogaart, C. H. Fahey, J. L. Leukemia-derived growth factor (non-interleukin 2) produced by a human malignant T lymphoid cell line. Proc Natl Acad Sci U S A. 1982; 79(22): 7004-8.

Jordan, S. C. Sakai, R. Malekzadeh, M. H. Pennisi, A. J. Ettenger, R. B. Uittenbogaart, C. H. Fine, R. N. Circulating immune complexes in pediatric renal allograft rejection.Transplantation. 1981; 31(3): 190-4.

Uittenbogaart, C. H. Fine, R. N. Diagnosis and treatment of allograft rejection. Paediatrician. 1981; 10(5-6): 400-8.

Jordan, S. C. Malekzadeh, M. H. Pennisi, A. J. Ettenger, R. B. Uittenbogaart, C. H. Fine, R. N. Accelerated acute rejection of primary renal allografts in pediatric patients.Transplantation. 1980; 30(1): 5-8.

Ettenger, R. B. Tong, M. J. Landing, B. H. Mosley, J. Malekzadeh, M. H. Pennisi, A. J. Uittenbogaart, C. H. Jordan, S. C. Wright, H. Fine, R. N. Hepatitis B infection in pediatric dialysis and transplant patients: significance of e antigen. J Pediatr. 1980; 97(4): 550-3.

Church, J. A. Uittenbogaart, C. Partial immunologic reconstitution and hyperimmunoglobulinemia-E in neonatally-acquired graft-versus-host disease. Ann Allergy. 1980; 44(4): 212-6.

Uittenbogaart, C. H. Robinson, B. J. Malekzadeh, M. H. Pennisi, A. J. Ettenger, R. B. Fine, R. N. Pretransplant T cell levels and renal allograft survival rates. Surgery. 1980; 87(4): 432-5.

Rizzoni, G. Malekzadeh, M. H. Pennisi, A. J. Ettenger, R. B. Uittenbogaart, C. H. Fine, R. N. Renal transplantation in children less than 5 years of age. Arch Dis Child. 1980; 55(7): 532-6.

Furler R.L. and Uittenbogaart C.H. GLI2 regulates TGF-â1 in Human CD4+ T-cells: Implications in Cancer and HIV Pathogenesis. PLoS One 2012; e40874: .

Karrich, J.J, Jachimowski, L.C.M., Nagasawa M., Kamp A, Balzarolo M, Wolkers M.C., Uittenbogaart C.H., van Ham S.M. and Blom B. IL-21 stimulated human plasmacytoid dendritic cells secrete Granzyme B, which impairs their capacity to induce T cell proliferation. Blood 2013; 121: 3103-3111.

Nixon, C.C., Vatakis, D.N., Reichelderfer, S.N., Dixit, D., Kim, S.G., Uittenbogaart, C.H. and Zack, J.A. HIV-1 Infection of Hematopoietic Progenitor Cells In Vivo. Blood 2013; 122: 2195-2204.

Karrich, J.J, Jachimowski, L.C.M., Libouban, M., Iyer, A.M., Brandwijk, K.I.M,, Taanman-Kueter, E.W., Nagasawa M., De Jong, E.C., Uittenbogaart C.H., and Blom B MicroRNA-146a regulates survival and maturation of human plasmacytoid dendritic cells. Blood 2013; 122: 3001-3009.

Wassner S J, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Fine R N Allograft survival in patients receiving anticonvulsant medications. Clinical nephrology. 1977; 8(1): 293-7.

Malekzadeh M H, Heuser E T, Ettenger R B, Pennisi A J, Uittenbogaart C H, Warshaw B L, Fine R N Focal glomerulosclerosis and renal transplantation. The Journal of pediatrics. 1979; 95(2): 249-54.

Fine R N, Edelbrock H H, Riddell H, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Korsch B M Renal transplantation in children. Urology. 1977; 9(6 Suppl): 61-71.

Fine R N, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Korsch B M Renal retransplantation in children. The Journal of pediatrics. 1979; 95(2): 244-8.

Epeldegui Marta, Blom Bianca, Uittenbogaart Christel H BST2/Tetherin is constitutively expressed on human thymocytes with the phenotype and function of Treg cells.European journal of immunology. 2015; 45(3): 728-37.

Fine R N, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Ettenger R B, Landing B H, Wright H T HBs antigenemia in renal allograft recipients. Annals of surgery. 1977; 185(4): 411-6.

Ettenger R B, Robinson B J, Uittenbogaart C H, Hacker T A, Pennisi A J, Malekzadeh M H, Fine R N Antibodies to donor B lymphocytes and autoantibodies in renal transplantation. Transplantation proceedings. 1979; 11(1): 401-3.

Ettenger R B, Uittenbogaart C H, Pennisi A J, Malekzadeh M H, Fine R N Long-term cadaver allograft survival in the recipient with a positive B lymphocyte crossmatch.Transplantation. 1979; 27(5): 315-8.

Karrich Julien J, Jachimowski Loes C M, Uittenbogaart Christel H, Blom Bianca The plasmacytoid dendritic cell as the Swiss army knife of the immune system: molecular regulation of its multifaceted functions. Journal of immunology (Baltimore, Md. : 1950). 2014; 193(12): 5772-8.

Ettenger R B, Terasaki P I, Ting A, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Fine R N Role of antibodies to B lymphocytes in renal transplantation.Transplantation proceedings. 1977; 9(1): 751-3.

Schut B J, Dooren L J, Uittenbogaart C H, Schellekens P T, Eijsvoogel V P Cellular immunity in patients with the Wiskott-Aldrich syndrome before and after administration of transfer factor: a follow-up study. Immunology. 1979; 36(1): 1-12.

Gurney Kevin B, Uittenbogaart Christel H Human immunodeficiency virus persistence and production in T-cell development. Clinical and vaccine immunology : CVI. 2006; 13(11): 1237-45.

Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Korsch B M, Fine R N, Main M E Current issues in pediatric renal transplantation. Pediatric clinics of North America. 1976; 23(4): 857-72.

Fine R N, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Negrete V F, Korsch B M Long-term results of renal transplantation in children. Proceedings of the Clinical Dialysis and Transplant Forum. 1977; 7(1): 117-20.

Ettenger R B, Robinson B, Louie J, Malekzadeh M H, Pennisi A J, Jordan S C, Uittenbogaart C H, Fine R N Autoantibodies in patients on dialysis awaiting renal transplantation. Proceedings of the Clinical Dialysis and Transplant Forum. 1979; 9(1): 205-8.

Gimeno Ramon, Weijer Kees, Voordouw Arie, Uittenbogaart Christel H, Legrand Nicolas, Alves Nuno L, Wijnands Erwin, Blom Bianca, Spits Hergen Monitoring the effect of gene silencing by RNA interference in human CD34+ cells injected into newborn RAG2-/- gammac-/- mice: functional inactivation of p53 in developing T cells.Blood. 2004; 104(13): 3886-93.

Radl J, Dooren L H, Morell A, Skvaril F, Vossen J M, Uittenbogaart C H Immunoglobulins and transient paraproteins in sera of patients with the Wiskott-Aldrich syndrome: a follow-up study. Clinical and experimental immunology. 1976; 25(2): 256-63.

Ettenger R B, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Jordan S C, Fine R N B lymphocyte crossmatching: lack of effect on transplant outcome based on incubation temperature. Proceedings of the Clinical Dialysis and Transplant Forum. 1979; 9(1): 197-200.

Baum L G, Pang M, Perillo N L, Wu T, Delegeane A, Uittenbogaart C H, Fukuda M, Seilhamer J J Human thymic epithelial cells express an endogenous lectin, galectin-1, which binds to core 2 O-glycans on thymocytes and T lymphoblastoid cells. The Journal of experimental medicine. 1995; 181(3): 877-87.

Dooren L J, de Koning J, Kamphuis R P, Uittenbogaart C H, Brubakk A M, Vossen J M [Bone marrow transplantation in patients with aplastic anemia]. Hämatologie und Bluttransfusion. 1975; 16(2): 330-51.

Jordan S C, Sakai R S, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Fine R N Circulating immune complexes in pediatric renal allograft recipients.Proceedings of the Clinical Dialysis and Transplant Forum. 1979; 9(1): 150-4.

Schmid I, Uittenbogaart C H, Giorgi J V Sensitive method for measuring apoptosis and cell surface phenotype in human thymocytes by flow cytometry. Cytometry. 1994; 15(1): 12-20.

Uittenbogaart C H, Robinson B J, Malekzadeh M H, Pennisi A J, Ettenger R B, Fine R N Pretransplant T cell levels and renal allograft survival. Proceedings of the European Dialysis and Transplant Association. European Dialysis and Transplant Association. 1979; 16(1): 449-53.

Hays E F, Kitada S, Uittenbogaart C H, Reeve J R Autocrine growth of murine lymphoma cells. Journal of the National Cancer Institute. 1988; 80(2): 116-21.

Pennisi A J, Ettenger R B, Costin G, Phillips L, Malekzadeh M H, Uittenbogaart C H, Fine R N Somatomedin activity and growth hormone concentration in pediatric renal allograft recipients. Transactions – American Society for Artificial Internal Organs. 1979; 25(1): 455-8.

Kanowith-Klein S, Saxon A, Uittenbogaart C H Constitutive production of B cell differentiation factor-like activity by human T and B cell lines. European journal of immunology. 1987; 17(5): 593-8.

Fine R N, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Korsch B M Retransplantation in children. Proceedings of the Clinical Dialysis and Transplant Forum. 1979; 8(1): 78-81.

Uittenbogaart C H, Fahey J L Leukemia derived growth factors. Lymphokine research. 1984; 3(2): 39-44.

Uittenbogaart C H, Fahey J L Leukemia-derived growth factor (non-interleukin 2) produced by a human malignant T lymphoid cell line. Proceedings of the National Academy of Sciences of the United States of America. 1982; 79(22): 7004-8.

Uittenbogaart C H, Isaacson A S, Stanley P, Pennisi A J, Malekzadeh M H, Ettenger R B, Fine R N Aseptic necrosis after renal transplantation in children. American journal of diseases of children (1960). 1978; 132(8): 765-7.

Warshaw B L, Edelbrock H H, Ettenger R B, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Fine R N Progression to end-stage renal disease in children with obstructive uropathy. The Journal of pediatrics. 1982; 100(2): 183-7.

Fine R N, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Negrete V F, Korsch B M Long-term results of renal transplantation in children. Pediatrics. 1978; 61(4): 641-50.

Ettenger R B, Opelz G, Walker J, Terasaki P I, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Fine R N Donor-specific preformed B-lymphocyte antibodies and mixed lymphocyte culture (MLC) blocking in cadaver renal allograft recipients. Transplantation proceedings. 1978; 10(2): 479-81.

Uittenbogaart C H, Fine R N Diagnosis and treatment of allograft rejection. Paediatrician. 1981; 10(5-6): 400-8.

Mentser M I, Clay S, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Fine R N Peripheral motor nerve conduction velocities in children undergoing chronic hemodialysis. Nephron. 1978; 22(4-6): 337-41.

Ettenger R B, Tong M J, Landing B H, Mosley J, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Jordan S C, Wright H, Fine R N Hepatitis B infection in pediatric dialysis and transplant patients: significance of e antigen.The Journal of pediatrics. 1980; 97(4): 550-3.

Malekzadeh M H, Pennisi A J, Phillips L, Ettenger R B, Uittenbogaart C H, Fine R N Growth and endocrine function in children with cystinosis following renal transplantation. Transactions – American Society for Artificial Internal Organs. 1978; 24(4-6): 278-81.

Rizzoni G, Malekzadeh M H, Pennisi A J, Ettenger R B, Uittenbogaart C H, Fine R N Renal transplantation in children less than 5 years of age. Archives of disease in childhood. 1980; 55(7): 532-6.

Ettenger R B, Heuser E T, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Fine R N Focal glomerulosclerosis in renal allografts: association with the nephrotic syndrome and chronic rejection. American journal of diseases of children (1960). 1977; 131(12): 1347-52.

Warshaw B L, Edelbrock H H, Ettenger R B, Malekzadeh M H, Pennisi A J, Uittenbogaart C H, Fine R N Renal transplantation in children with obstructive uropathy. The Journal of urology. 1980; 123(5): 737-41.

Malekzadeh M H, Neustein H B, Schneider J A, Pennisi A J, Ettenger R B, Uittenbogaart C H, Kogut M D, Fine R H Cadaver renal transplantation in children with cystinosis.The American journal of medicine. 1977; 63(4): 525-33.

Uittenbogaart C H, Robinson B J, Malekzadeh M H, Pennisi A J, Ettenger R B, Fine R N Use of antithymocyte globulin (dose by rosette protocol) in pediatric renal allograft recipients. Transplantation. 1979; 28(4): 291-3.

Satoh P, Elberg A, Davis J, Uittenbogaart C, Fine R, Hardy M A Effects of different ATG (ATGAM) regimens on levels of rosette-forming cells (RFC), serum horse IgG (HoI), and anti-horse antibodies in kidney transplant patients.Transplantation proceedings. 1979; 11(2): 1427-8.

Ettenger R B, Opelz G, Walker J, Terasaki P I, Uittenbogaart C, Pennisi A J, Malekzadeh M H, Fine R N Antibodies to donor B lymphocytes and mixed lymphocyte culture blocking in cadaveric renal transplantation.Transplantation. 1978; 25(4): 169-72.

Schoenberger Stephen P, Cheroutre Hilde, Uittenbogaart Christel, Marshak-Rothstein Ann The 2010 Midwinter Conference of Immunologists at Asilomar. Nature immunology. 2010; 11(5): 359-61.

Phillips L S, Pennisi A J, Belosky D C, Uittenbogaart C, Ettenger R B, Malekzadeh M H, Fine R N Somatomedin activity and inorganic sulfate in children undergoing hemodialysis. The Journal of clinical endocrinology and metabolism. 1978; 46(1): 165-8.

Merrill J E, Mohlstrom C, Uittenbogaart C, Kermaniarab V, Ellison G W, Myers L W Response to and production of interleukin 2 by peripheral blood and cerebrospinal fluid lymphocytes of patients with multiple sclerosis. Journal of immunology (Baltimore, Md. : 1950). 1984; 133(4): 1931-7.

Pennisi A J, Costin G, Phillips L S, Malekzadeh M M, Uittenbogaart C, Ettenger R B, Fine R N Somatomedin and growth hormone studies in pediatric renal allograft recipients who receive daily prednisone. American journal of diseases of children (1960). 1979; 133(9): 950-4.