Ubiquitin-proteasome-rich cytoplasmic structures in neutrophils of patients with Shwachman-Diamond syndrome

Haematologica. 2012 Jul;97(7):1057-63. doi: 10.3324/haematol.2011.048462. Epub 2012 Jan 22.

Abstract

Background: Shwachman-Diamond syndrome is an autosomal recessive disorder in which severe bone marrow dysfunction causes neutropenia and an increased risk of leukemia. Recently, novel particulate cytoplasmic structures, rich in ubiquitinated and proteasomal proteins, have been detected in epithelial cells and neutrophils from patients with Helicobacter pylori gastritis and several epithelial neoplasms.

Design and methods: Blood neutrophils from 13 cases of Shwachman-Diamond syndrome - ten with and three without SBDS gene mutation - and ten controls were investigated by confocal microscopy and ultrastructural immunocytochemistry using antibodies against ubiquitinated proteins, proteasomes, p62 protein, and Helicobacter pylori VacA, urease and outer membrane proteins.

Results: Many extensively disseminated particulate cytoplasmic structures, accounting for 22.78 ± 5.57% (mean ± standard deviation) of the total cytoplasm, were found in blood neutrophils from mutated Shwachman-Diamond syndrome patients. The particulate cytoplasmic structures showed immunoreactivity for polyubiquitinated proteins and proteasomes, but no reactivity for Helicobacter pylori products, which are present in particulate cytoplasmic structures of Helicobacter pylori-positive gastritis. Neutrophils from patients with Shwachman-Diamond syndrome frequently showed p62-positive autophagic vacuoles and apoptotic changes in 5% of cells. No particulate cytoplasmic structures were observed in most control neutrophils; however, in a few cells from two cases we noted focal development of minute particulate cytoplasmic structures, accounting for 0.74 ± 0.56% of the total cytoplasm (P<0.001 versus particulate cytoplasmic structures from mutated Shwachman-Diamond syndrome patients). Neutrophils from non-mutated Shwachman-Diamond-syndrome-like patients resembled controls in two cases, and a third case showed particulate cytoplasmic structure patterns intermediate between those in controls and those in mutated Shwachman-Diamond syndrome patients.

Conclusions: Particulate cytoplasmic structures are a prominent feature of neutrophils from patients with Shwachman-Diamond syndrome. They may help us to understand the mechanism of granulocyte dysfunction and the neoplastic risk of the disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Adolescent
  • Adult
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Bone Marrow / metabolism
  • Bone Marrow / pathology*
  • Bone Marrow Diseases / complications
  • Bone Marrow Diseases / genetics
  • Bone Marrow Diseases / pathology*
  • Child
  • Child, Preschool
  • Cytoplasmic Structures / genetics
  • Cytoplasmic Structures / metabolism*
  • Cytoplasmic Structures / ultrastructure
  • Exocrine Pancreatic Insufficiency / complications
  • Exocrine Pancreatic Insufficiency / genetics
  • Exocrine Pancreatic Insufficiency / pathology*
  • Female
  • Gene Expression
  • Humans
  • Immunohistochemistry
  • Lipomatosis / complications
  • Lipomatosis / genetics
  • Lipomatosis / pathology*
  • Male
  • Microscopy, Confocal
  • Mutation
  • Neutropenia / complications
  • Neutropenia / genetics
  • Neutropenia / pathology*
  • Neutrophils / metabolism*
  • Neutrophils / ultrastructure
  • Proteasome Endopeptidase Complex / genetics
  • Proteasome Endopeptidase Complex / metabolism*
  • Proteasome Endopeptidase Complex / ultrastructure
  • Proteins / genetics
  • Proteins / metabolism
  • Sequestosome-1 Protein
  • Shwachman-Diamond Syndrome
  • Ubiquitin / metabolism
  • Ubiquitinated Proteins / genetics
  • Ubiquitinated Proteins / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Bacterial Proteins
  • Proteins
  • SBDS protein, human
  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • Ubiquitin
  • Ubiquitinated Proteins
  • VacA protein, Helicobacter pylori
  • Proteasome Endopeptidase Complex