A Molecular Signature in Blood Reveals a Role for p53 in Regulating Malaria-Induced Inflammation

Immunity. 2019 Oct 15;51(4):750-765.e10. doi: 10.1016/j.immuni.2019.08.009. Epub 2019 Sep 3.

Abstract

Immunity that controls parasitemia and inflammation during Plasmodium falciparum (Pf) malaria can be acquired with repeated infections. A limited understanding of this complex immune response impedes the development of vaccines and adjunctive therapies. We conducted a prospective systems biology study of children who differed in their ability to control parasitemia and fever following Pf infection. By integrating whole-blood transcriptomics, flow-cytometric analysis, and plasma cytokine and antibody profiles, we demonstrate that a pre-infection signature of B cell enrichment, upregulation of T helper type 1 (Th1) and Th2 cell-associated pathways, including interferon responses, and p53 activation associated with control of malarial fever and coordinated with Pf-specific immunoglobulin G (IgG) and Fc receptor activation to control parasitemia. Our hypothesis-generating approach identified host molecules that may contribute to differential clinical outcomes during Pf infection. As a proof of concept, we have shown that enhanced p53 expression in monocytes attenuated Plasmodium-induced inflammation and predicted protection from fever.

Keywords: Plasmodium falciparum; RNA sequencing; RNA-seq; antibody profiling; flow cytometry; malaria; malaria immunity; prospective cohort study; systems biology; systems immunology; transcriptomics.

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Antibodies, Protozoan / metabolism
  • B-Lymphocytes / immunology*
  • Blood Proteins / metabolism*
  • Child
  • Child, Preschool
  • Disease Resistance
  • Female
  • Gene Expression Profiling
  • Humans
  • Infant
  • Inflammation / metabolism*
  • Interferons / metabolism
  • Malaria, Falciparum / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Plasmodium falciparum / physiology*
  • Prospective Studies
  • Receptors, Fc / metabolism
  • Signal Transduction
  • Th1 Cells / immunology*
  • Th2 Cells / immunology*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism*
  • Young Adult

Substances

  • Antibodies, Protozoan
  • Blood Proteins
  • Receptors, Fc
  • Tumor Suppressor Protein p53
  • Interferons