A non-BRICHOS surfactant protein c mutation disrupts epithelial cell function and intercellular signaling

BMC Cell Biol. 2010 Nov 20:11:88. doi: 10.1186/1471-2121-11-88.

Abstract

Background: Heterozygous mutations of SFTPC, the gene encoding surfactant protein C (SP-C), cause sporadic and familial interstitial lung disease (ILD) in children and adults. The most frequent SFTPC mutation in ILD patients leads to a threonine for isoleucine substitution at position 73 (I73T) of the SP-C preprotein (proSP-C), however little is known about the cellular consequences of SP-CI73T expression.

Results: To address this, we stably expressed SP-CI73T in cultured MLE-12 alveolar epithelial cells. This resulted in increased intracellular accumulation of proSP-C processing intermediates, which matched proSP-C species recovered in bronchial lavage fluid from patients with this mutation. Exposure of SP-CI73T cells to drugs currently used empirically in ILD therapy, cyclophosphamide, azathioprine, hydroxychloroquine or methylprednisolone, enhanced expression of the chaperones HSP90, HSP70, calreticulin and calnexin. SP-CI73T mutants had decreased intracellular phosphatidylcholine level (PC) and increased lyso-PC level without appreciable changes of other phospholipids. Treatment with methylprednisolone or hydroxychloroquine partially restored these lipid alterations. Furthermore, SP-CI73T cells secreted into the medium soluble factors that modulated surface expression of CCR2 or CXCR1 receptors on CD4+ lymphocytes and neutrophils, suggesting a direct paracrine influence of SP-CI73T on neighboring cells in the alveolar space.

Conclusion: We show that I73T mutation leads to impaired processing of proSP-C in alveolar type II cells, alters their stress tolerance and surfactant lipid composition, and activates cells of the immune system. In addition, we show that some of the mentioned cellular aspects behind the disease can be modulated by application of pharmaceutical drugs commonly applied in the ILD therapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Azathioprine / therapeutic use
  • Bronchoalveolar Lavage Fluid
  • CD4-Positive T-Lymphocytes / immunology
  • Calnexin / metabolism
  • Calreticulin / metabolism
  • Cell Line
  • Cyclophosphamide / therapeutic use
  • Epithelial Cells / metabolism*
  • HSP70 Heat-Shock Proteins / metabolism
  • HSP90 Heat-Shock Proteins / metabolism
  • Humans
  • Hydroxychloroquine / therapeutic use
  • Lung Diseases, Interstitial / drug therapy
  • Methylprednisolone / therapeutic use
  • Mice
  • Mutation
  • Phosphatidylcholines / metabolism
  • Pulmonary Surfactant-Associated Protein C / analysis
  • Pulmonary Surfactant-Associated Protein C / genetics
  • Pulmonary Surfactant-Associated Protein C / metabolism*
  • Receptors, CCR2 / metabolism
  • Receptors, Interleukin-8A / metabolism
  • Signal Transduction

Substances

  • Calreticulin
  • HSP70 Heat-Shock Proteins
  • HSP90 Heat-Shock Proteins
  • Phosphatidylcholines
  • Pulmonary Surfactant-Associated Protein C
  • Receptors, CCR2
  • Receptors, Interleukin-8A
  • SFTPC protein, human
  • Calnexin
  • Hydroxychloroquine
  • Cyclophosphamide
  • Azathioprine
  • Methylprednisolone