A human non-XLA immunodeficiency disease characterized by blockage of B cell development at an early ProB cell stage

Journal of Clinical Investigation

Volumn 98, Issue 7, 1996, Pages 1519-1526

  Meffre, E ^a   LeDeist, F ^b   De Saint Basile, G ^b   Deville, A ^c   Fougereau, M ^a   Fischer, A ^b   Schiff, C ^a  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b INSERM   (France)

^c Fondation Lenval Hopital pour Enfants   (France)

Author keywords

Btk; Ig genes; Pax 5; proB cells; surrogate light chain

Indexed keywords

ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; CASE REPORT; FEMALE; HUMAN; IMMUNE DEFICIENCY; IMMUNOGLOBULIN GENE; INFANT; PRE B LYMPHOCYTE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 0029818656     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118943     Document Type: Article

References (54)

1. Uckun, F.M., and J.A. Ledbetter. 1988. Immunobiologic differences between normal and leukemic human B-cell precursors. Proc. Natl. Acad. Sci. USA. 85:8603-8607.
2. Wormann, B., J.M. Anderson, J.A. Liberty, K. Galz-Peczalska, R.D. Brunning, T.L. Silberman, D.C. Arthur, and T.W. LeBien. 1989. Establishment of a leukemic cell model for studying human pre-B to B cell differentiation. J. Immunol. 142:110-117.
3. Alt, F.W., T.K. Blackwell, R.A. De Pinho, M.G. Reth, and M.D. Yancopoulos. 1986. Regulation of genome rearrangement events during lymphocyte differentiation. Immunol. Rev. 89:5-30.
4. Blackwell, T.K., and F.W. Alt. 1989. Mechanism and developmental program of immunoglobulin gene rearrangement in mammals. Annu. Rev. Genet. 23:605-636.
5. Dorshkind, K. 1994. Transcriptional control points during lymphopoiesis. Cell. 79:751-753.
6. Kerr, W.G., M.D. Cooper, L. Feng, P.D. Burrows, and L.M. Hendershot, 1989. μ heavy chains can associate with a pseudo light chain complex (ψL) in human pre-B cell lines. Int. Immunol. 1:355-361.
7. Hollis, G.F., G.A. Evans, J.M. Stafford-Hollis, S.J. Korsmeyer, and J.P. McKearn. 1989. Immunoglobulin λ light chain related genes 14.1 and 16.1 are expressed in pre-B cells and may encode the human immunoglobulin Ω light chain protein. Proc. Natl. Acad. Sci. USA. 86:5552-5556.
8. Bossy, D., M. Milili, J. Zucman, G. Thomas, M. Fougereau, and C. Schiff. 1991. Organisation and expression of the λ-like genes that contribute to the μ-ψ light chain complex in human pre-B cells. Int. Immunol. 3:1081-1090.
9. Sakaguchi, N., and F. Melchers. 1986. λ5, a new light chain related locus selectively expressed in pre-B lymphocytes. Nature (Lond.). 324:579-582.
10. Kudo, A., N. Sakaguchi, and F. Melchers. 1987. Organization of the murine Ig-related λ5 gene transcribed selectively in pre-B lymphocytes. EMBO (Eur. Mol. Biol. Organ.) J. 6:103-107.
11. Bauer, S.R., A. Kudo, and F. Melchers. 1988. Structure and preB lymphocyte restricted expression of the VpreB gene in humans and conservation of its structure in other mammalian species. EMBO (Eur. Mol. Biol. Organ.) J. 7:111-116.
12. pre-B/lambda5 surrogate light chain in early bone marrow precursor B cells of normal and B cell-deficient mutant mice. Cell. 77:133-143.
13. Winkler, T.H., A. Rolink, F. Melchers, and H. Karasuyama. 1995. Precursor B cells of mouse bone marrow express two different complexes with the surrogate light chain on the surface. Eur. J. Immunol. 25:446-450.
14. Guelpa-Fonlupt, V., C. Tonnelle, D. Blaise, M. Fougereau, and F. Fumoux. 1994. Discrete early pro-B and pre-B stages in normal human bone marrow as defined by surface pseudo-light chain expression. Eur. J. Immunol. 24: 257-264.
15. Nishimoto, N., H. Kubagawa, T. Ohno, G.I., Gartland, A.K. Stankovic, and M.D. Cooper. 1991. Normal pre-B cells express a receptor complex of μ heavy chains and surrogate light-chain proteins. Proc. Natl. Acad. Sci. USA. 88:6284-6288.
16. Lassoued, K., C.A. Nunez, L. Billips, H. Kubagawa, R.C. Monteiro, T.W. LeBien, and M.D. Cooper. 1993. Expression of surrogate light chain receptors is restricted to a late stage in pre-B cell differentiation. Cell. 73:73-86.
17. Bossy, D., J. Salamero, D. Olive, M. Fougereau, and C. Schiff. 1993. Structure, biosynthesis and transduction properties of the human μ-ψL complex: similar behavior of preB and intermediate preB-B cells in transducing ability. Int. Immunol. 5:467-478.
18. Nunez, C., N. Nishimoto, G.L. Gartland, L.G. Billips, P.D. Burrows, H. Kubagawa, and M.D. Cooper. 1996. B cells are generated throughout life in humans. J. Immunol. 156:866-872.
19. Campbell, K.S., E.J. Hager, R.J. Friedrich, and J.C. Cambier. 1991. IgM antigen receptor complex contains phosphoprotein products of B29 and mb-1 genes. Proc. Natl. Acad. Sci. USA. 88:3982-3986.
20. Sakaguchi, N., S. Kashiwamura, M. Kimoto, P. Thalmann, and F. Melchers. 1988. B lymphocyte lineage-restricted expression of mb-1, a gene with CD3-like structural properties. EMBO (Eur. Mol. Biol. Organ.) J. 7:3457-3464.
21. Hermanson, G.G., D. Eisenberg, P.W. Kincade, and R. Wall. 1988. B29: a member of the immunoglobulin gene superfamily exclusively expressed on beta-lineage cells. Proc. Natl. Acad. Sci. USA. 85:6890-6894.
22. Meffre, E., M. Fougereau, J.-N. Argenson, J.-M. Aubaniac, and C. Schiff. 1996. Cell surface expression of surrogate light chain (ψL) in the absence of μ on human proB cell lines and normal proB cells. Eur. J. Immunol. In press.
23. Conley, M.E. 1985. B cells in patients with X-linked agammaglobulinemia. J. Immunol. 134:3070-3074.
24. Vetrie, D., I. Vorechovsky, P. Sideras, J. Holland, A. Davies, F. Flinter, L. Hammarström, C. Kinnon, R. Levinsky, M. Bobrow, C.I.E. Smith, and D.R. Bentley. 1993. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases. Nature (Lond.). 361:226-233.
25. Tsukada, S., D.C. Saffran, D.J. Rawlings, O. Parolini, R. Cutler Allen, I. Klisak, R.S. Sparkes, H. Kubagawa, T. Mohandas, S. Quan, et al. 1993. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell. 72:279-290.
26. Milili, M., F. Le Deist, G. De Saint-Basile, A. Fischer, M. Fougereau, and C. Schiff. 1993. Bone marrow cells in X-linked agammaglobulinemia express pre-B-specific genes (lambda-like and V pre-B) and present immunoglobulin V-D-J gene usage strongly biased to a fetal-like repertoire. J. Clin. Invest. 91:1616-1629.
27. Conley, M.E., and S.K. Sweinberg. 1992. Females with a disorder phenotypically identical to X-linked agammaglobulinemia. J. Clin. Immunol. 12: 139-143.
28. De la Morena, M., R.N. Haire, Y. Ohta, R.P. Nelson, R.T. Litman, N.K. Day, R.A. Good, and G.W. Litman. 1995. Predominance of sterile immunoglobulin transcripts in a female phenotypically resembling Bruton's agammaglobulinemia. Eur. J. Immunol. 25:809-815.
29. Urbanek, P., Z.-Q. Wang, I. Fetka, E.F. Wagner, and M. Busslinger. 1994. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell. 79:901-912.
30. Allen, R.C., H.Y. Zoghbi, A.B. Moseley, H.M. Rosenblatt, and J.W. Belmont. 1992. Methylation of HpaII and HhaI sites near the polymorphic CAG repeat in the human androgen-receptor gene correlates with X chromosome inactivation. Am. J. Hum. Genet. 51:1229-1239.
31. Le Deist, F., G. Thoenes, J. Corado, B. Lisowska-Grospierre, and A. Fischer. 1991. Immunodeficiency with low expression of the T cell receptor/CD3 complex: effect on T lymphocytes activation. Eur. J. Immunol. 21:1641-1647.
32. Adams, B., P. Dörfler, A. Aguzzi, Z. Kozmik, P. Urbanek, I. Maurer-Fogy, and M. Busslinger. 1992. Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis. Genes Dev. 6:1589-1607.
33. Zhuang, Y., P. Soriano, and H. Weintraub. 1994. The helix-loop-helix gene E2A is required for B cell formation. Cell. 79:875-884.
34. Sun, X.-H. 1994. Constitutive expression of the IdI gene impairs mouse B cell development. Cell. 79:893-900.
35. Peschon, J.J., P.J. Morrissey, K.H. Grabstein, F.J. Ramsdell, E. Maraskovsky, B.C. Gliniak, L.S. Park, S.F. Ziegler, D.E. Williams, C.B. Ware, et al. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 180:1955-1960.
36. De Weers, M., M.C.M. Verschuren, M.E.M. Kraakman, R.G.J. Mensink, R.K.B. Schuurman, J.J.M. Van Dongen, and R.W. Hendriks. 1993. The Bruton's tyrosine kinase gene is expressed throughout B cell differentiation, from early precursor B cell stages preceding immunoglobulin gene rearrangement up to mature B cell stages. Eur. J. Immunol. 23:3109-3114.
37. Turner, M., P.J. Mee, P.S. Costello, O. Williams, A.A. Price, L.P. Duddy, M.T. Furlong, R.L. Geahlen, and V.L.J. Tybulewicz. 1995. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature (Lond.). 378:298-302.
38. Neale, G.A.M., and G.R. Kitchingman. 1991. mRNA transcripts initiating within the human immunoglobulin mu heavy chain enhancer region contain a non-translatable exon and are extremely heterogeneous at the 5′ end. Nucleic Acids Res. 19:2427-2433.
39. Thompson, A., E. Timmers, M.J.H. Kenter, M.E.M. Kraakman, R.W. Hendriks, and R.K.B. Schuurman. 1992. Immunoglobulin kappa light chain germ-line transcripts in human precursor B lymphocytes. Eur. J. Immunol. 22: 3167-3171.
40. H-Cμ transcription in human precursor B lymphocytes initiates in a unique region upstream of DQ52. Eur. J. Immunol. 25:257-261.
41. Vorechovsky, I., S. Koskinen, R. Paganelli, C.I.E. Smith, M. Busslinger, and L. Hammarström. 1995. The Pax5 gene: a linkage and mutation analysis in candidate human primary immunodeficiencies. Immunogenetics. 42:149-152.
42. Campana, D., J. Farrant, N. Inamdar, A.D.B. Webster, and G. Janossy. 1990. Phenotypic features and proliferative activity of B cell progenitors in X-linked agammaglobulinemia. J. Immunol. 145:1675-1680.
43. Khan, W.N., F.W. Alt, R.M. Gerstein, B.A. Malynn, I. Larsson, G. Rathbun, L. Davidson, S. Müller, A.B. Kantor, L.A. Herzenberg, et al. 1995. Defective B cell development and function in Btk-deficient mice. Immunity. 3:283-299.
44. Kerner, J.D., M.W. Appleby, R.N. Mohr, S. Chien, D.J. Rawlings, C.R. Maliszewski, O.N. Witte, and R.M. Perlmutter. 1995. Impaired expansion of mouse B cell progenitors lacking Btk. Immunity. 3:301-312.
45. Gong, S., and M.C. Nussenzweig. 1996. Regulation of an early developmental checkpoint in the B cell pathway by Igβ. Science (Wash. DC). 272:411-414.
46. Engel, P., L.-J. Zhou, D.C. Ord, S. Sato, B. Koller, and T.F. Tedder. 1995. Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity. 3:39-50.
47. Kozmik, Z., S. Wang, P. Dörfler, B. Adams, and M. Busslinger. 1992. The promoter of the CD19 gene is a target for the B-cell-specific transcription factor BSAP. Mol. Cell. Biol. 12:2662-2672.
48. Baker, S.J., and E.P. Reddy. 1995. B cell differentiation: role of E2A and Pax5/BSAP transcription factors. Oncogene. 11:413-426.
49. Busslinger, M., and P. Urbanek. 1995. The role of BSAP (Pax-5) in B-cell development. Curr. Opin. Genet. Dev. 5:595-601.
50. Sanyanusin, P., L.A. Schimmenti, L.A. McNoe, T.A. Ward, M.-E.M. Pierpont, M.J. Sullivan, W.B. Dobyns, and M.R. Eccles. 1995. Mutation of the Pax2 gene in a family with optic nerve colobomas, renal anomalies and vesicoureteral reflux. Nat. Genet. 9:358-364.
51. Li, Y.-S., K. Hayakawa, and R.R. Hardy. 1993. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178:951-960.
52. ten Boekel, E., F. Melchers, and A. Rolink. 1995. The status of Ig loci rearrangements in single cells from different stages of B cell development. Int. Immunol. 7:1013-1019.
53. Grawunder, U., T.M. J. Leu, D.G. Schatz, A. Werner, A.G. Rolink, F. Melchers, and T.H. Winkler. 1995. Down-regulation of RAG1 and RAG2 gene expression in preB cells after functional immunoglobulin heavy chain rearrangement. Immunity. 3:601-608.
54. Kitamura, D., A. Kudo, S. Schaal, W. Müller, F. Melchers, and K. Rajewsky. 1992. A critical role of lambda5 protein in B cell development. Cell. 69: 823-831.