Mutation of the hematopoietic cell phosphatase (Hcph) gene is associated with resistance to gamma-irradiation-induced apoptosis in Src homology protein tyrosine phosphatase (SHP)-1-deficient "motheaten" mutant mice

J Immunol. 2001 Jan 15;166(2):772-80. doi: 10.4049/jimmunol.166.2.772.

Abstract

To determine the role of Src homology protein tyrosine phosphatase (SHP-1) in the ionizing radiation-induced stress response, we analyzed the apoptotic response and cell cycle function in irradiated spleen cells of motheaten (me/me) mice. The defect in me/me mice has been attributed to mutations of the HCPH: gene, which encodes SHP-1. Homozygotes develop severe systemic autoimmune and inflammatory disease, whereas heterozygotes live longer and develop hematopoietic and lymphoid malignance. Spleen cells from C57BL/6 (B6)-me/me and B6-+/+ controls were analyzed after gamma-irradiation from a (137)Cs source. B6-me/me cells were significantly more resistant than B6-+/+ cells to gamma-irradiation-induced apoptosis exhibiting a higher LD(50). The defective apoptosis response of the B6-me/me cells was exhibited by T and B cells and macrophages. Of the Bcl-2 family members analyzed, a significant difference was observed in the transcription of Bax mRNA, which was up-regulated early after irradiation in B6-+/+ cells, but not B6-me/me cells. Analysis of 3,3'-dihexyloxacarbocyanine iodide revealed resistance to the gamma-irradiation-induced mitochondrial transmembrane permeability transition in the B6-me/me cells. The blocking of the cell cycle in the G(0)/G(1) phase characteristic of the irradiated B6-+/+ cells was not observed in the B6-me/me cells. There was decreased phosphorylation of p38 mitogen-activated protein kinase and increased phosphorylation of p53 from spleen cell lysates of irradiated B6-me/me mice compared with wild-type mice. These data suggest that SHP-1 plays an important role in regulation of apoptosis and cell cycle arrest after a gamma-irradiation-induced stress response.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Apoptosis / immunology
  • Apoptosis / radiation effects*
  • Cell Cycle / genetics
  • Cell Cycle / immunology
  • Cell Cycle / radiation effects
  • Cell Death / immunology
  • Cell Death / radiation effects
  • Cell Line
  • Gamma Rays*
  • Hybridomas
  • Immunity, Innate / radiation effects
  • Intracellular Membranes / radiation effects
  • Intracellular Signaling Peptides and Proteins
  • Membrane Potentials / radiation effects
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Mitochondria / radiation effects
  • Mitogen-Activated Protein Kinases / metabolism
  • Mitogen-Activated Protein Kinases / radiation effects
  • Mutation*
  • Permeability / radiation effects
  • Phosphorylation / radiation effects
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Protein Tyrosine Phosphatases / deficiency*
  • Protein Tyrosine Phosphatases / genetics*
  • Protein Tyrosine Phosphatases / metabolism
  • Protein Tyrosine Phosphatases / radiation effects
  • Proto-Oncogene Proteins / biosynthesis
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / radiation effects
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / radiation effects
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / radiation effects
  • SH2 Domain-Containing Protein Tyrosine Phosphatases
  • Spleen / cytology
  • Spleen / immunology
  • Spleen / radiation effects
  • Tumor Suppressor Protein p53 / metabolism
  • Tumor Suppressor Protein p53 / radiation effects
  • bcl-2-Associated X Protein
  • p38 Mitogen-Activated Protein Kinases
  • src Homology Domains / genetics*
  • src Homology Domains / immunology*
  • src Homology Domains / radiation effects

Substances

  • Bax protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • RNA, Messenger
  • Tumor Suppressor Protein p53
  • bcl-2-Associated X Protein
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Protein Tyrosine Phosphatases
  • Ptpn11 protein, mouse
  • Ptpn6 protein, mouse
  • SH2 Domain-Containing Protein Tyrosine Phosphatases