Interleukin-7 receptor α (IL-7Rα) deficiency: Cellular and molecular bases. Analysis of clinical, immunological, and molecular features in 16 novel patients

Immunological Reviews

Volumn 203, Issue , 2005, Pages 110-126

  Giliani, Silvia ^a   Mori, Luigi ^a   De Saint Basile, Geneviève ^b   Le Deist, Francoise ^b   Rodriguez Perez, Carmen ^a   Forino, Concetta ^a   Mazzolari, Evelina ^a   Dupuis, Sophie ^c   Elhasid, Ronit ^d   Kessel, Aharon ^d   Galambrun, Claire ^c   Gil, Juana ^e   Fischer, Alain ^b   Etzioni, Amos ^d   Notarangelo, Luigi D ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c HÔPITAL DEBROUSSE   (France)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 7 RECEPTOR ALPHA; RECOMBINASE; THYMIC STROMAL LYMPHOPOIETIN; UNCLASSIFIED DRUG;

ALPHA CHAIN; CLINICAL ARTICLE; CLINICAL FEATURE; COMBINED IMMUNODEFICIENCY; FEMALE; GENE; GENE MUTATION; GENE TARGETING; GENETIC ANALYSIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IL 7RALPHA GENE; IMMUNE DEFICIENCY; IMMUNOREACTIVITY; INFANT; INTERLEUKIN 7 RECEPTOR ALPHA DEFICIENCY; LYMPHOID CELL; LYMPHOID DEVELOPMENT; MALE; NEWBORN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; B-LYMPHOCYTES; CYTOKINES; FEMALE; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; MUTATION; RECEPTORS, INTERLEUKIN-7; SEVERE COMBINED IMMUNODEFICIENCY; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 19944433384     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2005.00234.x     Document Type: Review

References (113)

1. Fischer A. Severe combined immunodeficiencies (SCID). Clin Exp Immunol 2000;122:143-149.
2. Kaiman L, et al. Mutations in genes required for T-cell development: IL7R, CD45, IL2RG, JAK3, RAG1, RAG2, ARTEMIS, and ADA and severe combined immunodeficiency: HuGE Review. Genet Med 2003;6:16-26.
3. Buckley RH, et al. Hematopoietic stem-cell transplantation for the treatment of severe combined immunodeficiency. N Engl J Med 1999;340:508-516.
4. Cavazzana-Calvo M, et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 2000;288: 669-672.
5. Hacein-Bey-Abina S, et al. Sustained correction of X-linked severe combined immunodeficiency by ex vivo gene therapy. N Engl J Med 2002;346:1185-1193.
6. Aiuti A, et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 2002;296:2410-2413
7. Buckley RH. Primary immunodeficiency diseases due to defects in lymphocytes. N Engl J Med 2000;343:1313-1324.
8. Noguchi M, et al. Interleukin-2 receptor gamma chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 1993;73:147-157.
9. Puck JM, et al. The interleukin-2 receptor gamma chain maps to Xq13.1 and is mutated in X-linked severe combined immunodeficiency, SCIDX1. Hum Mol Genet 1993;2:1099-1104.
10. Leonard WJ, Shores EW, Love PE. Role of the common cytokine receptor gamma chain in cytokine signaling and lymphoid development. Immunol Rev 1995;148:97-114.
11. Asao H, et al. Cutting edge: the common gamma-chain is an indispensable subunit of the IL-21 receptor complex. J Immunol 2001;167:1-5.
12. Habib T, Senadheera S, Weinberg K, Kaushansky K. The common gamma chain (gamma c) is a required signaling component of the IL-21 receptor and supports IL-21-induced cell proliferation via JAK3. Biochemistry 2002;41:8725-8731.
13. Russell SM, et al. Mutation of Jak3 in a patient with SCID: essential role of Jak3 in lymphoid development. Science 1995;270:797-800.
14. Macchi P, et al. Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID). Nature 1995;377:65-68.
15. Lodolce JP, et al. IL-I5 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 1998;9:669-676.
16. von Freeden-Jeffry U, Vieira P, Lucian LA, McNeil T, Burdach SE, Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med 1995;181:1519-1526.
17. Peschon JJ, et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 1994;180: 1955-1960.
18. Grabstein KH, et al. Inhibition of murine B and T lymphopoiesis in vivo by an anti-interleukin 7 monoclonal antibody. J Exp Med 1993;178:257-264.
19. Fuel A, Leonard WJ. Mutations in the gene for the IL-7 receptor result in T(-)B(+)NK(+) severe combined immunodeficiency disease. Curr Opin Immunol 2000;12:468-473.
20. Roifman CM, Zhang J, Chitayat D, Sharfe N. A partial deficiency of interleukin-7R alpha is sufficient to abrogate T-cell development and cause severe combined immunodeficiency. Blood 2000;96:2803-2807.
21. Lynch M, Baker E, Park LS, Sutherland GR, Goodwin RG. The interleukin-7 receptor gene is at 5p13. Hum Genet 1992;89:566-568.
22. Teutsch SM, Booth DR, Bennetts BH, Heard RNS, Stewart GJ. Identification of 11 novel and common single nucleotide polymorphisms in the interleukin-7 receptor-α gene and their associations with multiple sclerosis. Eur J Hum Genet 2003;11:509-515.
23. Pleiman CM, Gimpel SD, Park LS, Harada H, Taniguchi T, Ziegler SF. Organization of the murine and human interleukin-7 receptor genes: two mRNAs generated by differential splicing and presence of a type I-interferon-inducible promoter. Mol Cell Biol 1991;11:3052-3059.
24. Venkitaraman A, Bowling R. Interleukin-7 functions by recruiting the tyrosine kinase p59fyn through a segment of its cytoplasmic tail. Proc Natl Acad Sci USA 1992;89: 12083-12087.
25. Lin J, et al. The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 1995;2:331-339.
26. Foxwell B, Beadling C, Guschin D, Kerr I, Cantrell D. Interleukin-7 can induce the activation of Jak1, Jak3 and STAT5 proteins in murine T cells. Eur J Immunol 1995;25:3041-3046.
27. Dadi H, Roifman C. Activation of phosphatidylinositol 3-kinase by ligation of the interleukin-7 receptor on human thymocytes. J Clin Invest 1993;92:1559-1563.
28. Seckinger P, Fougereau M. Activation of src family kinases in human pre-B cells by IL-7. J Immunol 1994;153:97-109.
29. fyn, two tyrosine kinases associated with the p90 interleukin-7 receptor in primary human T cells. Eur J Immunol 1995;25:2956-2960.
30. Soumelis V, Liu YJ. Human thymic stromal lymphopoietin: a novel epithelial cell-derived cytokine and a potential key player in the induction of allergic inflammation. Springer Semin Immunopathol 2004;25:325-333.
31. Leonard WJ. TSLP: finally in the limelight. Nat Immunol 2002;3:605-607.
32. Park LS, et al. Cloning of the murine thymic stromal lymphopoietin (TSLP) receptor: Formation of a functional heteromeric complex requires interleukin 7 receptor. J Exp Med 2000;192:659-670.
33. Namen AE, et al. Stimulation of B-cell progenitors by cloned murine interleukin-7. Nature 1988;333:571-573.
34. Conlon PJ, et al. Murine thymocytes proliferate in direct response to interleukin-7. Blood 1989;74:1368-1373.
35. Goodwin RG, et al. Human interleukin 7: Molecular cloning and growth factor activity on human and murine B-lineage cells. Proc Natl Acad Sci USA 1989;86:302-306.
36. Lai SY, Molden J, Goldsmith MA. Shared γc subunit within the human interleukin-7 receptor complex. A molecular basis for the pathogenesis of X-linked severe combined immunodeficiency. J Clin Invest 1997;99:169-177.
37. Kang J, SD. Cytokine functions in the formative stages of a lymphocyte's life. Curr Opin Immunol 2004;16:180-190.
38. Alexander WS. Suppressors of cytokine signaling (SOCS) in the immune system. Nat Rev Immunol 2002;2:410-416.
39. Matsumoto A, et al. Suppression of STAT5 functions in liver, mammary glands, and T cells in cytokine-inducible SH2-containing protein 1 transgenic mice. Mol Cell Biol 1999;19:6396-6407.
40. Chen M, et al. Complex effects of naturally occurring mutations in the JAK3 pseudokinase domain: evidence for interactions between the kinase and pseudokinase domains. Mol Cell Biol 2002;20:947-956.
41. Sudo T, Nishikawa S, Ohno N, Akiyama N, Tamakoshi M, Yoshida H. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc Natl Acad Sci USA 1993;90:9125-9129.
42. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997;91:661-672.
43. Mebius RE, et al. The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, CD45(+)CD4(+)CD3(-) cells, as well as macrophages. J Immunol 2001;166:6593-6601.
44. DeKoter RP, Lee H-J, Singh H. PU.1 regulates expression of the interleukin-7 receptor in lymphoid progenitors. Immunity 2002;16:297-309.
45. Yu Q, Erman B, Bhandoola A, Sharrow SO, Singer A. In vitro evidence that cytokine receptor signals are required for differentiation of double positive thymocytes into functionally mature CD8+ T cells. J Exp Med 2003;197:475-487.
46. Akashi K, Kondo M, von Freeden-Jeffry U, Murray R, Weissman IL. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 1997:89:1033-1041.
47. Matsuzaki N, Nakayama K, Tomita T, Isoda M, Loh DY, Nakauchi H. Role of bcl-2 in the development of lymphoid cells from the hematopoietic stem cell. Blood 1997;89: 853-862.
48. Wen R, et al. Jak3 selectively regulates Bax and Bcl-2 expression to promote T-cell development. Mol Cell Biol 2001;21: 678-689.
49. Khaled AR, et al. Bax deficiency partially corrects interleukin-7 receptor alpha deficiency. Immunity 2002;17:561-573.
50. Li WQ, Jiang Q, Khaled AR, Keller JR, Durum SK. Interleukin-7 inactivates the pro-apoptotic protein Bad promoting T cell survival. J Biol Chem 2004;279: 29160-29166.
51. Khaled AR, Kim K, Hofmeister R, Muegge K, Durum SK. Withdrawal of IL-7 induces Bax translocation from cytosol to mitochondria through a rise in intracellular pH. Proc Natl Acad Sci USA 1999;96:14776-14481.
52. Jiang Q, et al. Distinct regions of the interleukin-7 receptor regulate different Bcl2 family members. Mol Cell Biol 2004;24:6501-6513.
53. Trigueros C, et al. Pre-TCR signaling regulates IL-7 receptor α expression promoting thymocyte survival at the transition from the double-negative to double-positive stage. Eur J Immunol 2003;33:1968-1977.
54. Smart FM, Venkitaraman AR. Inhibition of interleukin 7 receptor signalling by antigen receptor assembly. J Exp Med 2000;191: 737-742.
55. Schlissel MS, Durum SD, Muegge K. The interleukin 7 receptor is required for T cell receptor gamma locus accessibility to the V(D)J recombinase. J Exp Med 2000;191:1045-1050.
56. Ye SK, et al. The IL-7 receptor controls the accessibility of the TCRgamma locus by Stat5 and histone acetylation. Immunity 2001;15:813-823.
57. Xiong N, Kang C, Raulet DH. Redundant and unique roles of two enhancer elements in the TCRγ locus in gene regulation and γδ T cell development. Immunity 2002;16:453-463.
58. Pallard C, Stegmann APA, van Kellefens T, Smart F, Venkitaraman A, Spits H. Distinct roles of the phosphatidylinositol 3-kinase and STAT5 pathways in IL-7-mediated development of human thymocyte precursors. Immunity 1999;10:525-535.
59. Porter BO, Scibelli P, Malek TR. Control of T cell development in vivo by subdomains within the IL-7 receptor α-chain cytoplasmic tail. J Immunol 2001;166:262-269.
60. Stoddart A, Fleming HE, Paige CJ. The role of the preBCR, the interleulcin-7 receptor, and homotypic interactions during B-cell development. Immunol Rev 2004;175:47-58.
61. Lee G, Namen AE, Gillis SW, Ellingsworth LR, Kincade PW. Normal B cell precursors responsive to recombinant murine IL-7 and inhibition of IL-7 activity by transforming growth factor-β. J Immunol 1989;142: 3875-3883.
62. Henderson AJ, Narayanan R, Collins L, Dorshkind K. Status of kappa L chain gene rearrangements and c-kit and IL-7 receptor expression in stromal cell-dependent pre-B cells. J Immunol 1992;149:1973-1979.
63. Chowdhury D, Sen R. Stepwise activation of the immunoglobulin mu heavy chain locus. EMBO J 2001;20:6394-6403.
64. Chowdhury D, Sen R. Transient IL-7/IL-7R signalling provides a mechanism for feedback inhibition of immunoglobulin heavy chain gene rearrangements. Immunity 2003;18:229-241.
65. Corcoran AE, Riddell A, Krooshop D, Venkitaraman AR. Impaired immunoglobulin gene rearrangement in mice lacking the IL-7 receptor. Nature 1998;391:904-907.
66. Suzuki H, et al. Xid-like immunodeficiency in mice with disruption of the p85alpha subunit of phosphoinositide 3-kinase. Science 1999;283:390-392.
67. Fruman DA, et al. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85alpha. Science 1999;283:393-397.
68. Clayton E, et al. A crucial role for the p110delta subunit of phosphatidylinositol 3-kinase in B cell development and activation. J Exp Med 2002;196:753-763.
69. Sexl V, et al. Stat5a/b contribute to interleukin 7-induced B-cell precursor expansion, but abl- and bcr/abl-induced transformation are independent of stat5. Blood 2000;96: 2277-2283.
70. Jameson SC. Maintaining the norm: T-cell homeostasis. Nat Rev Immunol 2002;2: 547-556.
71. Schluns KS, Kieper WC, Iameson SC, Lefrancois L. Interleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo. Nat Immunol 2001;1: 426-432.
72. Fry TJ, Mackall CL. Interleukin-7, master regulator of peripheral T-cell homeostasis? Trends Immunol 2001;22:564-571.
73. Tan JT, et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA 2001;98: 8732-8737.
74. Park J-H, et al. Suppression of IL7Rα transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 2004;21:289-302.
75. Seddon B, Zamoyska R. TCR and IL-7 receptor signals can operate independently or sinergize to promote lymphopenia-induced expansion of naïve T cells. J Immunol 2002;169:3752-3759.
76. Maraskovsky E, et al. Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J Immunol 1996;157:5315-5323.
77. Stockinger B, Barthlott T, Kassiotis G. The concept of space and competition in immune regulation. Immunology 2004;111:241-247.
78. Huster KM, et al. Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct memory T cell subsets. Proc Natl Acad Sci USA 2004;101:5610-5615.
79. Goldrath AW, et al. Cytokine requirements for acute and Basal homeostatic proliferation of naive and memory CD8+ T cells. J Exp Med 2002;195:1515-1522.
80. + T cell memory. Proc Natl Acad Sci USA 2004;101:9357-9362.
81. Lali FV, Crawley J, McCulloch DA, Foxwell BMJ. A late, prolonged activation of phopshatidylinositol 3-kinase pathway is required for T cell proliferation. J Immunol 2004;172:3527-3534.
82. Pandey A, et al. Cloning of a receptor subunit required for signaling by thymic stromal lymphopoietin. Nat Immunol 2000;1:59-64.
83. Friend SL, Hosier S, Nelson A, Foxworthe D. Williams DE, Farr A. A thymic stromal cell line supports in vitro development of surface IgM+ B cells and produces a novel growth factor affecting B and T lineage cells. Exp Hematol 1994;22:321-328.
84. Sims JE, et al. Molecular cloning and biological characterization of a novel murine lymphoid growth factor. J Exp Med 2000;192:671-680.
85. Quentmeier H, et al. Cloning of human thymic stromal lymphopoietin (TSLP) and signaling mechanisms leading to proliferation. Leukemia 2001;15: 1286-1292.
86. Reche PA, et al. Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J Immunol 2001;167: 336-343.
87. Fujio K, et al. Molecular cloning of a novel type 1 cytokine receptor similar to the common gamma chain. Blood 2000;95:2204-2211.
88. Tonozuka Y, Fujio K, Sugiyama T, Nosaka T, Hirai M, Kitamura T. Molecular cloning of a human novel type 1 cytokine receptor related to δ1/TSLPR. Cytogenet Cell Genet 2001;93:23-25.
89. Isaksen DE, Baumann H, Trobridge PA, Farr AG, Levin SD, Ziegler SF. Requirement for Stat5 in thymic stromal lymphopoietin-mediated signal transduction. J Immunol 1999;163:5971-5977.
90. Isaksen DE, et al. Uncoupling of proliferation and Stat5 activation in thymic stromal lymphopoietin-mediated signal transduction. J Immunol 2002;168: 3288-3294.
91. Carpino N, et al. Absence of an essential role for thymic stromal lymphopoietin receptor in murine B-cell development. Mol Cell Biol 2004;24:2584-2592.
92. Levin SD, et al. Thymic stromal lymphopoietin: a cytokine that promotes the development of IgM+ B cells in vitro and signals via a novel mechanism. J Immunol 1999;162:677-683.
93. Watanabe N, et al. Human thymic stromal lymphopoietin promotes dendritic cell-mediated CD4+ T cell homeostatic expansion. Nat Immunol 2004;5:426-434.
94. Gilliet M, et al. Human dendritic cells activated by TSLP and CD40L induce proallergic cytotoxic T cells. J Exp Med 2003;197:1059-1063.
95. Vosshenrich CAJ, Cumano A, Müller W, Di Santo JP, Vieira P. Thymic stromal-derived lymphopoietin distinguishes fetal from adult B cell development. Nat Immunol 2003;4:773-779.
96. Vosshenrich CAJ, Cumano A, Müller W, Di Santo JP, Vieira P. Pre-B cell receptor expression in necessary for thymic stromal lymphopoietin responsiveness in the bone marrow but not in the liver environment. Proc Natl Acad Sci USA 2004;101: 11070-11075.
97. Al-Shami A, et al. A role for thymic stromal lymphopoietin in CD4+ T cell development. J Exp Med 2004;200:159-168.
98. Osborn MJ, Ryan PL, Kirchhof N, Panoskaltsis-Mortari A, Mortari F, Tudor K-SRS. Overexpression of murine TSLP impairs lymphopoiesis and myelopoiesis. Blood 2004;103:843-851.
99. He YW, Malek TR. Interleukin-7 receptor alpha is essential for the development of gamma delta + T cells, but not natural killer cells. J Exp Med 1996;184:289-293.
100. Adachi S, et al. Essential role of IL-7 receptor α in the formation of Peyer's patch anlage. Int Immunol 1998;10:1-6.
101. Cao X, et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor γ chain. Immunity 1995;2:223-238.
102. Di Santo JP, Muller W, Guy-Grand D, Fischer A, Rajewsky K. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor γ chain. Proc Natl Acad Sci USA 1995;92: 377-381.
103. Nosaka T, et al. Defective lymphoid development in mice lacking Jak3. Science 1995;270:800-802.
104. Thomis DC, Gurniak CB, Tivol E, Sharpe AH, Berg LJ. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 1995;270:794-797.
105. Puel A, Ziegler SF, Buckley RH, Leonard WJ. Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency. Nat Genet 1998;20:394-397.
106. Elhasid R, Bergman R, Etzioni A. Autoimmunity in severe combined immunodeficiency (SCID). Blood 2002;100:2677-2678.
107. Hilton DJ, Watowich SS, Katz L, Lodish HF. Saturation mutagenesis of the WSXWS motif of the erythropoietin receptor. J Biol Chem 1996;271:4699-4708.
108. Antoine C, et al. Long-term survival and transplantation of haemopoietic stem cells for immunodeficiencies: report of the European experience 1968-99. Lancet 2003;361:553-560.
109. Myers LA, Patel DD, Puck JM, Buckley RH. Hematopoietic stem cell transplantation for severe combined immunodeficiency in the neonatal period leads to superior thymic output and improved survival. Blood 2002;99:872-878.
110. Bartolome J, et al. B cell function after haploidentical in utero bone marrow transplantation in a patient with severe combined immunodeficiency. Bone Marrow Transplant 2002;29:625-628.
111. Haddad E, et al. Long-term chimerism and B-cell function after bone marrow transplantation in patients with severe combined immunodeficiency with B cells: a single-center study of 22 patients. Blood 1999;94:2923-2930.
112. Griscelli C, Durandy A, Ballet JJ, Prieur AM, Hors J. T- and B-cell chimerism in two patients with severe combined immunodeficiency (SCID) after transplantation. Transplant Proc 1977;IX:171-175.
113. Laffort C, et al. Severe cutaneous papillomavirus disease after haemopoietic stem-cell transplantation in patients with severe combined immune deficiency caused by common gammac cytokine receptor subunit of JAK-3 deficiency. Lancet 2004;363:2051-2054.