Monoallelic expression of Pax5: A paradigm for the haploinsufficiency of mammalian Pax genes?

Biological Chemistry

Volumn 380, Issue 6, 1999, Pages 601-611

  Nutt, Stephen L ^a   Busslinger, Meinrad ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

B cell development; Haploinsufficiency; Monoallelic expression; Pax5; Single cell RT PCR

Indexed keywords

ALLELE; B LYMPHOCYTE; DEVELOPMENTAL GENETICS; DIPLOIDY; DOMINANT GENE; GENE MUTATION; GENETIC DISORDER; GENETIC ENGINEERING; GENETIC TRANSCRIPTION; IMMUNOGENETICS; MAMMAL; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; RECESSIVE GENE; REVIEW;

ALLELES; ANIMALS; B-CELL-SPECIFIC ACTIVATOR PROTEIN; B-LYMPHOCYTES; CELL LINEAGE; DNA-BINDING PROTEINS; HAPLOTYPES; HETEROZYGOTE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MODELS, GENETIC; NUCLEAR PROTEINS; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 0032996437     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.1999.077     Document Type: Review

References (63)

1. Adams, B., Dörfler, P., Aguzzi, A., Kozmik, Z., Urbánek, P., Maurer-Fogy, I., and Busslinger, M. (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.
2. Bain, G., and Murre, C. (1998). The role of E-proteins in B- and T-lymphocyte development. Sem. Immunol. 10, 143-153.
3. Bain, G., Maandag, E.C.R., Izon, D.J., Amsen, D., Kruisbeek, A.M., Weintraub, B.C., Krop, I., Schlissel, M.S., Feeney, A.J., van Roon, M., van der Valk, M., te Riele, H.P.J., Berns, A., and Murre, C. (1994). E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79, 885-892.
4. Baldwin, C.T., Hoth, C.F., Amos, J.A., da-Silva, E.O., and Milunsky, A. (1992). An exonic mutation in the HuP2 paired domain gene causes Waardenburg's syndrome. Nature 355, 637-638.
5. Barlow, D.P. (1995). Gametic imprinting in mammals. Science 270, 1610-1613.
6. + T cells. Science 281, 1352-1354.
7. Bopp, D., Burri, M., Baumgartner, S., Frigerio, G., and Noll, M. (1986). Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell 47, 1033-1040.
8. Busslinger, M., Klix, N., Pfeffer, P., Graninger, P.G., and Kozmik, Z. (1996). Deregulation of PAX-5 by translocation of the Eμ enhancer of the IgH locus adjacent to two alternative PAX-5 promoters in a diffuse large-cell lymphoma. Proc. Natl. Acad. Sci. USA 93, 6129-6134.
9. Callaerts, P., Halder, G., and Gehring, W.J. (1997). Pax-6 in development and evolution. Annu. Rev. Neurosci. 20, 483-532.
10. Chess, A., Simon, I., Cedar, H., and Axel, R. (1994). Allelic inactivation regulates olfactory receptor gene expression. Cell 78, 823-834.
11. Cline, T.W. (1993). The Drosophila sex determination signal: how do flies count to two? Tends Genet. 9, 385-390.
12. Czerny, T., Schaffner, G., and Busslinger, M. (1993). DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site. Genes Dev. 7, 2048-2061.
13. Engelkamp, D., and van Heyningen, V. (1996). Transcription factors in disease. Curr. Opin. Genet. Dev. 6, 334-342.
14. 2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 67, 767-774.
15. Fisher, E., and Scambler, P. (1994). Human haploinsufficiency -one for sorrow, two for joy. Nature Genet. 7, 5-7.
16. Forejt, J., and Gregorová, S. (1992). Genetic analysis of genomic imprinting: an imprintor-1 gene controls inactivation of the paternal copy of the mouse Tme locus. Cell 70, 443-450.
17. Georgopoulos, K., Moore, D.D., and Derfler, B. (1992). Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science 258, 808-812.
18. Gorman, J.R., van der Stoep, N., Monroe, R., Cogne, M., Davidson, L., and Alt, F.W. (1996). The Igκ 3′ enhancer influences the ratio of Igκ versus Igλ B lymphocytes. Immunity 5, 241-252.
19. Hanson, I., and van Heyningen, V. (1995). Pax6: more than meets the eye. Trends Genet. 11, 268-272.
20. Hanson, I.M., Fletcher, J.M., Jordan, T., Brown, A., Taylor, D., Adams, R.J., Punnett, H.H., and van Heyningen, V. (1994). Mutations at the PAX6 locus are found in heterogeneous anterior segment malformations including Peters' anomaly. Nature Genet. 6, 168-173.
21. Held, W., and Raulet, D.H. (1997). Expression of the Ly49A gene in murine natural killer cell clones is predominantly but not exclusively mono-allelic. Eur. J. Immunol. 27, 2876-2884.
22. Held, W., and Kunz, B. (1998). An allele-specific, stochastic gene expression process controls the expression of multiple Ly49 family genes and generates a diverse, MHC-specific NK cell receptor repertoire. Eur. J. Immunol. 28, 2407-2416.
23. Held, W., Roland, J., and Raulet, D.H. (1995). Allelic exclusion of Ly49-family genes encoding class I MHC-specific receptors on NK cells. Nature 376, 355-358.
24. Hill, R.E., Favor, J., Hogan, B.L., Ton, C.C., Saunders, G.F., Hanson, I.M., Prosser, J., Jordan, T., Hastie, N.D., and van Heyningen, V. (1991). Mouse Small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522-525.
25. Holländer, G.A., Zuklys, S., Morel, C., Mizoguchi, E., Mobisson, K., Simpson, S., Terhorst, C., Wishart, W., Golan, D.E., Bhan, A.K., and Burakoff, S.J. (1998). Monoallelic expression of the interleukin-2 locus. Science 279, 2118-2121.
26. Hu, M., Krause, D., Greaves, M., Sharkis, S., Dexter, M., Heyworth, C., and Enver, T. (1997). Multilineage gene expression precedes commitment in the hematopoietic system. Genes Dev. 11, 774-785.
27. Johnson, C.V., Singer, R.H., and Lawrence, J.B. (1991). Fluorescent detection of nuclear RNA and DNA: Implications for genome organization. Methods Cell Biol. 35, 73-99.
28. Keller, S.A., Jones, J.M., Boyle, A., Barrow, L.L., Killen, P.D., Green, D.G., Kapousta, N.V., Hitchcock, P.F., Swank, R.T., and Meisler, M.H. (1994). Kidney and retinal defects (Krd), a transgene-induced mutation with adeletion of mouse chromosome 19 that includes the Pax2 locus. Genomics 23, 309-320.
29. Komori, T., Yagi, H., Nomura, S., Yamaguchi, A., Sasaki, K., Deguchi, K., Shimizu, Y., Bronson, R.T., Gao, Y.-H., Inada, M., Sato, M., Okamoto, R., Kitamura, Y., Yoshiki, S., and Kishimoto, T. (1997). Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89, 755-764.
30. Kozmik, Z., Wang, S., Dörfler, P., Adams, B., and Busslinger, M. (1992). The promoter of the CD19 gene is a target for the B-cell-specific transcription factor BSAP. Mol. Cell. Biol. 12, 2662-2672.
31. Lee, B., Thirunavukkarasu, K., Zhou, L., Pastore, L., Baldini, A., Hecht, J., Geoffroy, V., Ducy, P., and Karsenty, G. (1997). Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nature Genet. 16, 307-310.
32. Long, E.O., and Wagtmann, N. (1997). Natural killer cell receptors. Curr. Opin. Immunol. 9, 344-350.
33. Macchia, P.E., Lapi, P., Krude, H., Pirro, M.T., Missero, C., Chiovato, L., Souabni, A., Baserga, M., Tassi, V., Pinchera, A., Fenzi, G., Grüters, A., Busslinger, M., and Di Lauro, R. (1998). PAX8 mutations associated with congenital hypothyroidism caused by thyroid dysgenesis. Nature Genet. 19, 83-86.
34. Mansouri, A., Hallonet, M., and Gruss, P. (1996). Pax genes and their roles in cell differentiation and development. Curr. Opin. Cell Biol. 8, 851-857.
35. Mundlos, S., Otto, F., Mundlos, C., Mulliken, J.B., Aylsworth, A.S., Albright, S., Lindhout, D., Cole, W.G., Henn, W., Knoll, J.H.M., Owen, M.J., Mertelsmann, R., Zabel, B.U., and Olsen, B.R. (1997). Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89, 773-779.
36. Noll, M. (1993). Evolution and role of Pax genes. Curr. Opin. Genet. Dev. 3, 595-605.
37. Nutt, S.L., Urbánek, P., Rolink, A., and Busslinger, M. (1997). Essential functions of Pax5 (BSAP) in pro-B cell development: difference between fetal and adult B lymphopoiesis and reduced V-to-DJ recombination at the IgH locus. Genes Dev. 11, 476-491.
38. Nutt, S.L., Morrison, A.M., Dörfler, P., Rolink, A., and Busslinger, M. (1998). Identification of BSAP (Pax-5) target genes in early B-cell development by loss- and gain-of-function experiments. EMBO J. 17, 2319-2333.
39. Nutt, S.L., Vambrie, S., Steinlein, P., Kozmik, Z., Rolink, A., Weith, A., and Busslinger, M. (1999). Independent regulation of the two Pax5 alleles during B-cell development. Nature Genet. 21, 390-395.
40. Olson, E.N., Arnold, H.-H., Rigby, P.W.J., and Wold, B.J. (1996). Know your neigbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 85, 1-4.
41. Otto, F., Thornell, A.P., Crompton, T., Denzel, A., Gilmour, K.C., Rosewell, I.R., Stamp, G.W.H., Beddington, R.S.P., Mundlos, S., Olsen, B.R., Selby, P.B., and Owen, M.J. (1997). Cbfa1, a candidate geneforcleidocranial dysplasiasyndrome, is essential for osteoblast differentiation and bone development. Cell 89, 765-771.
42. Panning, B., and Jaenisch, R. (1996). DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev. 10, 1991-2002.
43. Parkhurst, S.M., and Meneely, P.M. (1994). Sex determination and dosage compensation: lessons from flies and worms. Science 264, 924-932.
44. Read, A. P. (1995). Pax genes - Paired feet in three camps. Nature Genet. 9, 333-334.
45. Rivière, I., Sunshine, M.J., and Littman, D.R. (1998). Regulation of IL-4 expression by activation of individual alleles. Immunity 9, 217-228.
46. Sanyanusin, P., Schimmenti, L.A., McNoe, L.A., Ward, T.A., Pierpont, M.E.M., Sullivan, M.J., Dobyns, W.B., and Eccles, M.R. (1995). Mutation of the PAX2 gene in a family with optic nerve colombomas, renal anomalies and vesicoureteral reflux. Nature Genet. 9, 358-364.
47. Schedl, A., Ross, A., Lee, M., Engelkamp, D., Rashbass, P., van Heyningen, V., and Hastie, N.D. (1996). Influence of PAX6 gene dosage on development: overexpression causes severe eye abnormalities. Cell 86, 71-82.
48. Schwarz, M., Alvarez-Bolado, G., Urbánek, P., Busslinger, M., and Gruss, P. (1997). Conserved biological function between Pax-2 and Pax-5 in midbrain and cerebellum development: Evidence from targeted mutation. Proc. Natl. Acad. Sci. USA 94, 14518-14523.
49. Strachan, T., and Read, A.P. (1994). PAX genes. Curr. Opin. Genet. Dev. 4, 427-438.
50. Sun, X.-H. (1994). Constitutive expression of the Id1 gene impairs mouse B cell development. Cell 79, 893-900.
51. Tassabehji, M., Read, A.P., Newton, V.E., Harris, R., Balling, R., Gruss, P., and Strachan, T. (1992). Waardenburg's syndrome patients have mutations in the human homologue of the Pax-3 paired box gene. Nature 355, 635-636.
52. Ton, C.C.T., Hirvonen, H., Miwa, H., Weil, M.M., Monaghan, P., Jordan, T., van Heyningen, V., Hastie, N.D., Meijers-Heijboer, H., Drechsler, M., Royer-Pokora, B., Collins, F., Swaroop, A., Strong, L.C., and Saunders, G.F. (1991). Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region. Cell 67, 1059-1074.
53. Urbánek, P., Wang, Z.-Q., Fetka, I., Wagner, E.F., and Busslinger, M. (1994). Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79, 901-912.
54. Urbánek, P., Fetka, I., Meisler, M.H., and Busslinger, M. (1997). Cooperation of Pax2 and Pax5 in midbrain and cerebellum development. Proc. Natl. Acad. Sci. USA 94, 5703-5708.
55. Vorechovsky, I., Koskinen, S., Paganelli, R., Smith, E.C.I., Busslinger, M., and Hammarström, L. (1995). The PAX5 gene: a linkage and mutation analysis in candidate human primary immunodeficiencies. Immunogenet. 42, 149-152.
56. Walther, C., and Gruss, P. (1991). Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
57. Watanabe, D., and Barlow, D.P. (1996). Random and imprinted monoallelic expression. Genes Cells 1, 795-802.
58. Wijgerde, M., Grosveld, F., and Fraser, P. (1995). Transcription complex stability and chromatin dynamics in vivo. Nature 377, 209-213.
59. Wilkie, A.O.M. (1994). The molecular basis of genetic dominance. J. Med. Genet. 31, 89-98.
60. Wilm, B.E.D., Peters, H., Balling, R., and Imai, K. (1998). Targeted disruption of Pax1 defines its null phenotype and proves haploinsufficiency. Proc. Natl. Acad. Sci. USA 95, 8692-8697.
61. Xu, W., Rould, M.A., Jun, S., Desplan, C., and Pabo, C.O. (1995). Crystal structure of the paired domain-DNA complex at 2.5 Å resolution reveals structural basis for Pax developmental mutations. Cell 80, 639-650.
62. Zhou, L.-J., Ord, D.C., Hughes, A.L., and Tedder, T.F. (1991). Structure and domain organization of the CD19 antigen of human, mouse, and guinea pig B lymphocytes. J. Immunol. 147, 1424-1432.
63. Zhuang, Y., Soriano, P., and Weintraub, H. (1994). The helix-loop-helix gene E2A is required for B cell formation. Cell 79, 875-884.