Epidermal Langerhans cell development and differentiation

Immunobiology

Volumn 198, Issue 5, 1998, Pages 588-605

  Strobl, Herbert ^a   Riedl, Elisabeth ^a   Bello Fernandez, Concha ^a   Knapp, Walter ^a,b  

^a UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; TUMOR NECROSIS FACTOR ALPHA;

BONE MARROW CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL STRUCTURE; ECTODERM; EPIDERMIS CELL; HEMATOPOIETIC SYSTEM; HUMAN; HUMAN CELL; LANGERHANS CELL; PRIORITY JOURNAL; REVIEW;

EID: 0031940525     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0171-2985(98)80080-6     Document Type: Article

References (99)

1. STEINMAN, R. M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9: 271.
2. LANGERHANS, P. 1868. Über die Nerven der menschlichen Haut. Virchows Arch. Pathol. Anat. Physiol. 44: 325.
3. STINGL, G. 1993. The skin: initiation and target site of immune responses. Recent Results Cancer Res. 128: 45.
4. WOLFF, K. 1972. The Langerhans Cell. Curr. Probl. Derm. 4: 79.
5. PRUNIERAS, M. 1969. Interactions between keratinocytes and dendritic cells. J. Invest. Derm. 52: 1.
6. STINGL, G., E. C. WOLFF-SCHREINER, W. J. PICHLER, F. GSCHNAIT, W. KNAPP and K. WOLFF. 1977. Epidermal Langerhans cells bear Fc and C3 receptors. Nature 268: 245.
7. STINGL, G., S. I. KATZ, L. CLEMENT, I. GREEN and E. M. SHEVACH. 1978. Immunologicl functions of Ia-bearing epidermal Langerhans cells. J. Immunol. 121: 2005.
8. BIRBECK, M. S. C., A. S. BREATHNACH and J. D. EVERALL. 1961. An electron microscopy study of basal melanocyte and high level clear cell (Langerhans cell) in vitiligo. J. Invest. Dermatol. 73: 51.
9. KASHIHARA, M., M. UEDA, Y. HORIGUCHI, F. FURUKAWA, M. HANAOKA and S. IMAMURA. 1986. A monoclonal antibody specifically reactive to human Langerhans cells. J. Invest. Derm. 87: 602.
10. FITHIAN, E., P. KUNG, G. GOLDSTEIN, M. RUBENFELD, C. FENGOGLIO and R. EDELSON. 1981. Reactivity of Langerhans cells with hybridoma antibody. Proc. Natl. Acad. Sci. USA 78: 2541.
11. OGOU, S.-I., C. YOSHIDA-NORO and M. TAKEICHI. 1983. Calcium-dependent cell-cell adnesion molecules common to hepatocytes and teratocarcinoma stem cells. J. Cell Biol. 97: 944.
12. SCHMITT, D. A., D. HANAU, T. BIEBER, C. DEZUTTER-DAMBUYANT, D. SCHMITT, M. FABRE, G. PAULY and J.-P. CAZENAVE. 1990. Human epidermal Langerhans cells express only the 40-kilodalton Fey Receptor (FcRII). J. Immunol. 144: 4284.
13. TANG, A., M. AMAGAI, L. G. GRANGER, J. R. STANLEY and M. C. UDEY. 1993. Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 361: 82.
14. KATZ, S. I., K. TAMAKI and D. H. SACHS. 1979. Epidermal Langerhans cells are derived from cells originating in the bone marrow. Nature 282: 324.
15. VOLC-PLATZER, B., G. STINGL, K. WOLFF, W. HINTERBERGER and W. SCHNEDL. 1984. Cytogenetic identification of allogeneic epidermal Langerhans cells in a bone marrow-graft recipient. N. Eng. J. Med. 310: 1123.
16. WOOD, G. S., R. R. TURNER, R. A. SHIURBA, L. ENGL and R. A. WARNKE. 1985. Human dendritic cells and macrophages. Am. J. Pathol. 119: 73.
17. STINGL, G., and P. R. BERGSTRESSER. 1995. Dendritic cells: a major story unfolds. Immunology Today 16: 330.
18. DE PANFILIS, G., D. SOLIGO, G. C. MANARA, C. FERRARI and C. TORRESANI. 1989. Adhesion molecules on the plasma membrane of epidermal cells. I. Human resting Langerhans cells express two members of the adherence-promoting CD11/CD18 family, namely, H-Mac-1 (CD11b/CD18) and gp 150,95 (CD11c/CD18). J. Invest. Dermatol. 93: 60.
19. CAUX, C., C. DEZUTTER-DAMBUYANT, D. SCHMITT and J. BANCHEREAU. 1992. GM-CSF and TNF-a cooperate in the generation of dendritic Langerhans cells. Nature 360: 258.
20. FRANKLIN, W. A., D. Y. MASON, K. PULFORD, B. FALINI, E. BLISS, K. C. GATTER, H. STEIN, L. C. CLARKE and J. O. MCGEE. 1986. Immunohistological Analysis of human mononuclear phagocytes and dendritic cells by using monoclonal antibodies. Lab. Invest. 54: 322.
21. REIS E SOUSA, C., P. D. STAHL and J. M. AUSTYN. 1993. Phagocytosis of antigens by Langerhans cells in vitro. J. Exp. Med. 178: 509.
22. MOLL, H. 1993. Experimental cutaneous leishmaniasis: Langerhans cells internalize Leishmania major and induce an antigen-specific T-cell response. Adv. Exp. Biol. 329: 587.
23. + progenitors in human bone marrow. J. Immunol. 149: 2681.
24. SANTIAGO-SCHWARZ, F., E. BELJLOS, B. DIAMOND and S. E. CARSONS. 1992. TNF in combination with GM-CSF enhances the differentiation of neonatal cord blood stem cells into dendritic cells and macrophages. J. Leukoc. Biol. 52: 274.
25. + bone marrow progenitors that are expanded by c-kit-ligand and yield pure dendritic cell colonies in the presence of granulocyte/macrophage colony-stimulating factor and tumor necrosis factor alpha. J. Exp. Med. 182: 1111.
26. MACKENSEN, A., B. HERBST, G. KÖHLER, G. WOLFF-VORBECK F. M. ROSENTHAL H. VEELKEN, P. KULMBURG, H. E. SCHAEFER, R. MERTELSMANN and A. LINDEMANN. 1995. Delineation of the dendritic cell lineage by generating large numbers of Birbeck granule-positive Langerhans cells from human peripheral blood progenitor cells in vitro. Blood 86: 2699.
27. + hematopoietic progenitor cells in cancer patients. Eur. J. Immunol. 26: 595.
28. + hematopoietic precursor cells. Blood 87: 535.
29. + hematopoietic progenitor cells. Blood 87: 1292.
30. + hemopoietic progenitors. J. Immunol. 157: 1499.
31. REID, C. D. L., P. R. FRYER, C. CLIFFORD, A. KIRK, J. TIKERPAE and S. C. KNIGHT. 1990. Identification of hematopoietic progenitors of macrophages and dendritic Langerhans cells (DL-CFU) in human marrow and peripheral blood. Blood 76: 1139.
32. STROBL, H., C. BELLO-FERNANDEZ, E. RIEDL, W. F. PICKL, O. MAJDIC, S. D. LYMAN and W. KNAPP. 1997. flt3 Ligand in cooperation with TGF-β1 potentiates in vitro development of Langerhans type dendritic cells in serum-free medium. Blood 90: 1425.
33. GALY, A., M. TRAVIS, D. CEN and B. CHEN. 1995. Human T, B, natural killer cells, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 3: 459.
34. dim cells in the human thymus can differentiate into T, natural killer, and dendritic cells but are distinct from pluripotent stem cells. Blood 87: 5196.
35. GROUARD, G., M.-C. RISSOAN, L. FILGUEIRA, I. DURAND, J. BANCHEREAU and Y.-J. LIU. 1997. The enigmatic plasmacytoid T cells develop into dendritic cells with Interleukin (IL)-3 and CD40-Ligand. J. Exp. Med. 185: 1101.
36. +linperipheral blood cells with dendritic precursor characteristics. Submitted.
37. + hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF+TNF-α. J. Exp. Med. 184: 695.
38. SZABOLCS, P., D. AVIGAN, S. GEZELTER, D. H. CIOCON, M. A. S. MOORE, R. M. STEINMAN and J. W. YOUNG. 1996. Dendritic cells and macrophages can mature independently from a human bone marrow-derived, post-colony-forming unit intermediate. Blood 87: 4520.
39. + human hemopoietic progenitor cells. Ann. Hematol. 281.
40. + hemopoietic progenitor cells. Blood 86: 4115.
41. STRUNK, D., C. EGGER, G. LEITNER, D. HANAU and G. STINGL. 1997. A skin homing molecule defines the Langerhans cell progenitor in human blood. J. Exp. Med. 185: 1131.
42. FREUDENTHAL, P. S. and R. M. STEINMAN. 1990. The distinct surface of human blood dendritic cells, as observed after an improved isolation method. Proc. Natl. Acad. Sci. USA 87: 7698.
43. THOMAS, R., L. S. DAVIS and P. E. LIPSKY. 1993. Isolation and characterization of human peripheral blood dendritic cells. J. Immunol. 150: 821.
44. O'DOHERTY, U., R. M. STEINMAN, M. PENG, P. U. CAMERON, S. GEZELTER, I. KOPELOFF, W. J. SWIGGARD, M. POPE and N. BHARDWAJ. 1993. Dendritic cells freshly isolated from human blood express CD4 and mature into typical immunostimulatory dendritic cells after culture in monocyte-conditioned medium. J. Exp. Med. 178: 1067.
45. O'DOHERTY, U., M. PENG, S. GEZELTER, W. J. SWIGGARD, M. BETJES, N. BHARDWAJ and R. M. STEINMAN. 1994. Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 82: 487.
46. THOMAS, R., and P. E. LIPSKY. 1994. Human peripheral blood dendritic cell subsets. Isolation and characterization of precursors and mature antigen-presenting cells. J. Immunol. 153: 4016.
47. ZHOU, L. J., and T. F. TEDDER. 1995. Human blood dendritic cells selectively express CD83, a member of the immunoglobulin superfamily. J. Immunol. 154: 3821.
48. WEISSMAN, D., Y. LI, J. ANANWORANICH, L.-J. Zhou, J. ADELSBERGER, T. F. TEDDER, M. BASELER and A. S. FAUCI. 1995. Three populations of cells with dendritic morphology exist in peripheral blood, only one of which is infectable with human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 92: 826.
49. MAURER, D., E. FIEBIGER, C. EBNER, B. REININGER, G. F. FISCHER, S. WICHLAS, M.-H. JOUVIN, M. SCHMITT-EGENOLF, D. KRAFT, J.-P. KINET and G. STINGL. 1996. Peripheral blood dendritic cells express FceRI as a complex composed of FceRIg- and FceRIg-chains and can use this receptor for IgE-mediated allergen presentation. J. Immunol 157: 607.
50. + precursors. J. Immunol. 2134.
51. STROBL, H., C. SCHEINECKER, B. CSMARITS, O. MAJDIC and W. KNAPP. 1995. Flow cytometric analysis of intracellular CD68 molecule expression in normal and malignant haematopoiesis. Br. J. Haematol. 90: 774.
52. GROUARD, G., I. DURAND, L. FILGUEIRA, J. BANCHEREAU and Y.-J. LIU. 1996. Dendritic cells capable of stimulating T cells in germinal centers. Nature 384: 364.
53. LENNERT, K., E. KAISERLING and H. K. MÜLLER-HERMELINK. 1975. T-associated plasma cells. Lancet 1: 1031.
54. FACCHETTI, F., C. DE WOLF-PEETERS, D. Y. MASON, K. PULFORD, J. J. VAN DEN OORD and V. J. DESMET. 1988. Plasmacytoid T cells: immunohistochemical evidence for their monocyte/macrophage origin. Am. J. Pathol. 133: 15.
55. STEINMAN, R. M., M. PACK and K. INABA. 1997. Dendritic cells in the T-cell areas of lymphoid organs. Immunol. Rev. 156: 25.
56. PETERS, J. H., S. RUHL and D. FRIEDRICHS. 1987. Veiled accessory cells deduced from monocytes. Immunobiol. 176: 154.
57. PETERS, J. H., J. RUPPERT, R. K. H. GIESELER, H. M. NAJAR and H. XU. 1990. Differentiation of human monocytes into CD14 negative accessory cells: Do dendritic cells derive from the monocytic lineage? Pathobiology 59: 122.
58. ROSSI, G., N. HEVEKER, B. THIELE, H. GELDERBLOM and F. STEINBACH. 1992. Development of a Langerhans cell phenotype from peripheral blood monocytes. Immunol. Lett. 31: 189.
59. KASINRERK, W., T. BAUMRUKER, O. MAJDIC, W. KNAPP and H. STOCKINGER. 1993. CD1 molecule expression on human monocytes induced by granulocyte-macrophage colony-stimulating factor. J. Immunol. 150: 579.
60. RUPPERT, J., C. SCHUTT, D. OSTERMEIER and J. H. PETERS. 1993. Down-regulation and release of CD14 on human monocytes by IL-4 depends on presence of serum or GM-CSF. Adv. Exp. Med. Biol. 329: 281
61. SALLUSTO, F., and A. LANZAVECCHIA. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus Interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179: 1109.
62. ROMANI, N., S. GRUNER, D. BRANG, E. KÄMPGEN, A. LENZ, B. TROCKENBACHER, G. KONWALINKA, P. O. FRITSCH, R. M. STEINMAN and G. SCHULER. 1994. Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 180: 83.
63. PETERS, J. H., R. GIESELER, B. THIELE and F. STEINBACH. Dendritic cells: from ontogenetic orphans to myelomonocytic descendants. Immunol. Today 17: 273.
64. + peripheral blood monocytes. J. Immunol. 157: 3850.
65. + dendritic cells. Proc. Natl. Acad. Sci. USA 93: 2588.
66. + leukocytes acquire the phenotype and function of antigen-presenting dendritic cells when cultured in GM-CSF and IL-4. J. Leuk. Biol. 59: 208.
67. + bone marrow precursors cultured with c-kit ligand, granulocyte-macrophage colony-stimulating factor, and TNF-α. J. Immunol. 154: 5851.
68. + hematopoietic progenitor cells. Blood 87: 2376.
69. + hematopoietic progenitors induces their proliferation and differentiation into functional dendritic cells. J. Exp. Med. 185: 341.
70. CHILDS, C. B., J. A. PROPER, R. F. TUCKER and H. L. MOSES. 1982. Serum contains a platelet-derived transforming growth factor. Proc. Natl. Acad. Sci. USA 79: 5312.
71. MASSAGUÉ, J., L. ATTISANO and J. L. WRANA. 1994. The TGF-β family and its composite receptors. Trends in Cell Biol. 4: 172.
72. CASHMAN, J. D., A. C. EAVES, E. W. RAINES, R. Ross and C. J. EAVES. 1990. Mechanisms that regulate the cell cycle status of very primitive hematopoietic cells in long-term human marrow cultures. I. Stimulatory role of a variety of mesenchymal cell activators and inhibitory role of TGF-β. Blood 75: 96.
73. HATZFELD, J., M. L. LI, E. L. BROWN, H. SOOKDEA, J. P. LEVESQUE, T. O'TOOLE, C. GURNEY, S. C. CLARK and A. HATZFELD. 1991. Release of early human hematopoietic progenitors from quiescence by antisense transforming growth factor b1 or Rb oligonicleotides. J. Exp. Med. 174: 925.
74. +++ stem/progenitor cells from human bone marrow and umbilical cord blood plated with and without serum. Exp. Hematology 21: 1442.
75. KELLER, J. R., S. H. BARTELMEZ, E. SITNICKA, F. W. RUSCETTI, M. ORTIZ, J. M. GOOYA and S. E. W. JACOBSEN. 1994. Distinct and overlapping direct effects of macrophage inflammatory protein-1a and transforming growth factor β on hematopoietic progenitor/stem cell growth. Blood 84: 2175.
76. + human hematopoietic progenitor cells through different cell kinetic mechanisms depending on the applied stimulus. Exp. Hematol. 22: 903.
77. JACOBSEN, F. W, T. STOKKE and S. E. W. JACOBSEN. 1995. Transforming growth factor-β potently inhibits the viability-promoting activity of stem cell factor and other cytokines and induces apoptosis of primitive murine hematopoietic progenitor cells. Blood 86: 2957.
78. KELLER, J. R., S. E. W. JACOBSEN, K. T. SILL, L. R. ELLINGSWORTH and F. W. RUSCETTI. 1991. Stimulation of granulopoiesis by transforming growth factor β: Synergy with granulocyte/macrophage-colony-stimulating factor. Proc. Natl. Acad. Sci. USA 88: 7190.
79. PIABICELLO, W., D. FERRERO, F. SANAVIO, R. BADONI, A. STACCHINI, A. SEVERINO and M. AGLIETTA. 1991. Responsiveness of highly enriched CFU-GM subpopulations from bone marrow, peripheral blood, and cord blood to hemopoietic growth inhibitors. Exp. Hematol. 19: 1084.
80. CELADA, A., and R. A. MAKI. 1992. Transforming growth factor-β enhances the M-CSF- and GM-CSF-stimulated proliferation of macrophages. J. Immunol. 148: 1102.
81. BURSUKER I., K. M. NEDDERMANN, B. A. PETTY, B. SCHACTER, G. L. SPITALNY, M. A. TEPPER and R. D. PASTERNAK. 1992. In vivo regulation of hemopoiesis by transforming growth factor beta 1: Stimulation of GM-CSF- and M-CSF-dependent murine bone marrow precursors. Exp. Hematol. 20: 431.
82. DE BENEDETTI, F., L. A. FALK, L. R. ELLINGSWORTH, F. W. RUSCETTI and C. R. Faltynek. 1990. Synergy between transforming growth factor-β and tumor necrosis factor-a in the induction of monocytic differentiation of human leukemic cell lines. Blood 75: 626.
83. KAMIJO, R., K. TAKEDA, M. NAGUMO and K. KONNO. 1990. Effects of combinations of transforming growth factor-β, and tumor necrosis factor on induction of differentiation of human myelogenous leukemic cell lines. J. Immunol. 144: 1311.
84. KRYSTAL, G., V. LAM, W. DRAGOWSKA, C. TAKAHASHI, J. APPEL, A. GONTIER, A. JENKINS H. LAM, L. QUON and P. LANSDORP. 1994. Transforming growth factor β1 is an inducer of erythroid differentiation. J. Exp. Med. 180: 851.
85. RIEDL, E., H. STROBL, O. MAJDIC and W. KNAPP. 1997. TGF-β1 promotes in vitro generation of dendritic cells by protecting progenitor cells from apoptosis. J. Immunol. 158: 1591.
86. LARDON, F., H.-W. SNOECK, G. NIJS, M. LENJOU, M. E. PEETERMANS I. RODRIGUS, Z. N. BERNEMAN and D. R. VAN BOCKSTAELE. 1994. Transforming growth factor-β regulates the cell cycle status of interleukin-3 (IL-3) plus IL-1, stem cell factor, or IL-6 stimulated CD34 human hematopoietic progenitor cells through different cell kinetic mechanisms depending on the applied stimulus. Exp. Hematol. 22: 903.
87. JACOBSEN F. W., T. STOKKE and S. E. W. JACOBSEN. 1995. Transforming growth factor-β potently inhibits the viability-promoting activity of stem cell factor and other cytokines and induces apoptosis of primitive murine hematopoietic progenitor cells. Blood 86: 2957.
88. SNOECK, H.-W., S. WEEKX, A. MOULIJN, F. LARDON, M. LENJOU, G. NYS, P. C. F. VAN RANST, D. R. VAN BOCKSTAELE and Z. N. BERNEMAN. 1996. Tumor necrosis factor a is a potent synergistic factor for the proliferation of primitive human hematopoietic progenitor cells and induces resistance to transforming growth factor β but not to Interferon γ. J. Exp. Med. 183: 705.
89. LYMAN, S. D., L. JAMES, T. V. Bos, P. DE VRIES, K. BRASEL, B. GLINIAK, L. T. HOLLINGSWORTH, K. S. PICHA, H. J. MCKENNA, R. R. SPLETT, F. A FLETCHER, E. MARASKOVSKY, T. FARRAH, F. D., D. E. WILLIAMS and M. P. BECKMAN. 1993. Molecular cloning of a ligand for the flt3/flk-2 tyrosine kinase receptor: A proliferate factor for primitive hematopoietic cells. Cell 75: 1157.
90. HANNUM, C., J. CULPEPPER, D. CAMPBELL, T. MCCLANAHAN, S. ZURAWSKI, J. F. BAZAN, R. KASTELEIN, S. HUDAK, J. WAGNER, J. MATTSON, J. LUH, G. DUDA, N. MARTINA, T. PETERSON, S. MENON, A. SHANAFELT, M. MUENCH, G. KELNER, R. NAMIKAWA, D. RENNICK, M.-G. RONCARLO, A. ZLOTNIK, O. ROSNET, P. DUBREUIL, D. BIRNBAUM and F. LEE. 1994. Ligand for FLT3/FLK2 receptor tyrosine kinase regulates growth of hematopoietic stem cells and is encoded by variant RNAs. Nature 368: 643.
91. LYMAN, S. D., L. JAMES, L. JOHNSON, K. BRASEL, P. DE VRIES, S. S. ESCPBAR, H. DOWNEY, R. R. SPLETT, M. P. BECKMANN and H. J. MCKENNA. 1994. Cloning of the human homologue of the murine flt3 ligand: A growth factor for early hematopoietic progenitor cells. Blood 83: 2795.
92. MATTHEWS, W., C. T. JORDAN, G. W. WIEGAND, D. PARDOLL and I. R. LEMISCHKA. 1991. A receptor tyrosine kinase specific to hematopoietic stem and progenitor cell-enriched populations. Cell 65: 1143.
93. ROSNET, O., S. MARCHETTO, O. DELAPEYRIERE and D. BIRNBAUM 1991. Murine flt3, a gene encoding a novel tyrosine kinase receptor of the PDGFR/CSF1R family. Oncogene 6: 1641
94. MARASKOVSKI, E., K. BRASEL, M. TEEPE, E. R. Roux, S. D. LYMAN, K. SHORTMAN and H. J. MCKENNA. 1996. Dramatic increase in the numbers of functionally mature dendritic cells in flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J. Exp. Med. 184: 1953.
95. RAPPOLD I., B. L. ZIEGLER, I. KÖHLER, S. MARCHETTP, O. ROSNET, D. BIRNBAUM, P. J. SIMMONS, A. C. W. ZANETTINO, B. HILL, S. NEU, W. KNAPP, R. ALITALO, K. ALITALO, A. ULLRICH, L. KANZ and H.-J. BÜHRING. 1997. Functional and phenotypic characterization of cord blood and bone marrow subsets expressing FLT3 (CD135) receptor tyrosme kinase. Blood 90: 111.
96. GABBIANELLI, M., E. PELOSI, E. MONTESORO, M. VALTIERI, L. LUCHETTI, P. SAMOGGIA, L. VITELLI, T. BARBERI, U. TESTA, S. LYMAN and C. PESCHLE. 1995. Multi-level effects of flt3 Ligand on human hematogoiesis: expansion of putative stem cells and proliferation ot granulomonocytic progenitors/monocytic precursors. Blood 85: 1661.
97. BORKOWSKI, T. A., J. J. LETTERIO, A. G. FARR and M. C. UDEY. 1996. A role for endogenous transforming growth factor b1 in Langerhans cell biology: the skin of transforming growth factor β1 null mice is devoid of epidermal Langerhans cells. J. Exp. Med. 184: 2417.
98. SCHULL, M. M., I. ORMSBY, A. B. KIER, S. PAWLOWSKI, R. J DIEBOLD, M. YIN, R. ALLEN, C. SIDMAN, G. PROETZEL, D. CALVIN, N. ANNUNZIATA and T. DOETSCHMAN. 1992. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359: 693.
99. BOIVIN, G. P., B. A. O'TOOLE, I. E. ORSMY, R. J. DIEBOLD, M. J. EIS, T. DOETSCHMAN and A. B. KIER. 1995. Onset and progression of pathological lesions in transforming growth factor-β1-deficient mice. Am. J. Pathol. 146: 276.