Multisystem Anomalies in Severe Combined Immunodeficiency with Mutant BCL11B

N Engl J Med. 2016 Dec 1;375(22):2165-2176. doi: 10.1056/NEJMoa1509164.

Abstract

Background: Severe combined immunodeficiency (SCID) is characterized by arrested T-lymphocyte production and by B-lymphocyte dysfunction, which result in life-threatening infections. Early diagnosis of SCID through population-based screening of newborns can aid clinical management and help improve outcomes; it also permits the identification of previously unknown factors that are essential for lymphocyte development in humans.

Methods: SCID was detected in a newborn before the onset of infections by means of screening of T-cell-receptor excision circles, a biomarker for thymic output. On confirmation of the condition, the affected infant was treated with allogeneic hematopoietic stem-cell transplantation. Exome sequencing in the patient and parents was followed by functional analysis of a prioritized candidate gene with the use of human hematopoietic stem cells and zebrafish embryos.

Results: The infant had "leaky" SCID (i.e., a form of SCID in which a minimal degree of immune function is preserved), as well as craniofacial and dermal abnormalities and the absence of a corpus callosum; his immune deficit was fully corrected by hematopoietic stem-cell transplantation. Exome sequencing revealed a heterozygous de novo missense mutation, p.N441K, in BCL11B. The resulting BCL11B protein had dominant negative activity, which abrogated the ability of wild-type BCL11B to bind DNA, thereby arresting development of the T-cell lineage and disrupting hematopoietic stem-cell migration; this revealed a previously unknown function of BCL11B. The patient's abnormalities, when recapitulated in bcl11ba-deficient zebrafish, were reversed by ectopic expression of functionally intact human BCL11B but not mutant human BCL11B.

Conclusions: Newborn screening facilitated the identification and treatment of a previously unknown cause of human SCID. Coupling exome sequencing with an evaluation of candidate genes in human hematopoietic stem cells and in zebrafish revealed that a constitutional BCL11B mutation caused human multisystem anomalies with SCID and also revealed a prethymic role for BCL11B in hematopoietic progenitors. (Funded by the National Institutes of Health and others.).

Publication types

  • Case Reports

MeSH terms

  • Abnormalities, Multiple / genetics*
  • Animals
  • Brain / diagnostic imaging
  • Cell Movement
  • Disease Models, Animal
  • Gene Expression Regulation
  • Hematopoietic Stem Cell Transplantation
  • Hematopoietic Stem Cells / metabolism
  • Hematopoietic Stem Cells / physiology*
  • Humans
  • In Vitro Techniques
  • Infant, Newborn
  • Magnetic Resonance Imaging
  • Male
  • Mutation, Missense*
  • Neonatal Screening / methods
  • Receptors, Antigen, T-Cell
  • Repressor Proteins / deficiency
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism
  • Severe Combined Immunodeficiency / genetics*
  • Tumor Suppressor Proteins / deficiency
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism
  • Zebrafish / growth & development

Substances

  • BCL11B protein, human
  • Receptors, Antigen, T-Cell
  • Repressor Proteins
  • Tumor Suppressor Proteins