Quantitative Lipidomics in Pulmonary Alveolar Proteinosis

Am J Respir Crit Care Med. 2019 Oct 1;200(7):881-887. doi: 10.1164/rccm.201901-0086OC.

Abstract

Rationale: Pulmonary alveolar proteinosis (PAP) is characterized by filling of the alveolar spaces by lipoprotein-rich material of ill-defined composition, and is caused by molecularly different and often rare diseases that occur from birth to old age.Objectives: To perform a quantitative lipidomic analysis of lipids and the surfactant proteins A, B, and C in lavage fluids from patients with proteinosis of different causes in comparison with healthy control subjects.Methods: During the last two decades, we have collected BAL samples from patients with PAP due to autoantibodies against granulocyte-macrophage colony-stimulating factor; genetic mutations in CSF2RA (colony-stimulating factor 2 receptor α-subunit), MARS (methionyl aminoacyl-tRNA synthetase), FARSB (phenylalanine-tRNA synthetase, β-subunit), and NPC2 (Niemann-Pick disease type C2); and secondary to myeloid leukemia. Their lipid composition was quantified.Measurements and Main Results: Free cholesterol was largely increased by 60-fold and cholesteryl esters were increased by 24-fold. There was an excessive, more than 130-fold increase in ceramide and other sphingolipids. In particular, the long-chain ceramides d18:1/20:0 and d18:1/24:0 were elevated and likely contributed to the proapoptotic environment observed in PAP. Cellular debris lipids such as phosphatidylethanolamine and phosphatidylserine were only moderately increased, by four- to sevenfold. The surfactant lipid class phosphatidylcholine expanded 17-fold, lysophosphatidylcholine expanded 54-fold, and the surfactant proteins A, B, and C expanded 144-, 4-, and 17-fold, respectively. These changes did not differ among the various diseases that cause PAP.Conclusions: This insight into the alveolar lipidome may provide monitoring tools and lead to new therapeutic strategies for PAP.

Keywords: BAL; lipids; pulmonary alveolar proteinosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Apoptosis
  • Autoimmune Diseases / metabolism
  • Bronchoalveolar Lavage Fluid
  • Case-Control Studies
  • Ceramides / metabolism
  • Child
  • Child, Preschool
  • Cholesterol / metabolism
  • Cholesterol Esters / metabolism
  • Female
  • Genetic Diseases, X-Linked / genetics
  • Genetic Diseases, X-Linked / metabolism
  • Humans
  • Infant
  • Leukemia, Myeloid / complications
  • Lipid Metabolism*
  • Lipidomics*
  • Male
  • Methionine-tRNA Ligase / genetics
  • Middle Aged
  • Phenylalanine-tRNA Ligase / genetics
  • Phosphatidylcholines / metabolism
  • Phosphatidylethanolamines / metabolism
  • Phosphatidylserines / metabolism
  • Pulmonary Alveolar Proteinosis / etiology
  • Pulmonary Alveolar Proteinosis / genetics
  • Pulmonary Alveolar Proteinosis / metabolism*
  • Pulmonary Surfactant-Associated Protein A / metabolism
  • Pulmonary Surfactant-Associated Protein B / metabolism
  • Pulmonary Surfactant-Associated Protein C / metabolism
  • Pulmonary Surfactant-Associated Proteins / metabolism*
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor / genetics
  • Sphingolipids / metabolism
  • Vesicular Transport Proteins / genetics
  • Young Adult

Substances

  • CSF2RA protein, human
  • Ceramides
  • Cholesterol Esters
  • NPC2 protein, human
  • Phosphatidylcholines
  • Phosphatidylethanolamines
  • Phosphatidylserines
  • Pulmonary Surfactant-Associated Protein A
  • Pulmonary Surfactant-Associated Protein B
  • Pulmonary Surfactant-Associated Protein C
  • Pulmonary Surfactant-Associated Proteins
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor
  • Sphingolipids
  • Vesicular Transport Proteins
  • phosphatidylethanolamine
  • Cholesterol
  • MARS1 protein, human
  • Methionine-tRNA Ligase
  • Phenylalanine-tRNA Ligase

Supplementary concepts

  • Pulmonary Alveolar Proteinosis, Acquired
  • Surfactant Metabolism Dysfunction, Pulmonary, 4