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Evolution of the primate trypanolytic factor APOL1.

Russell Thomson1, Giulio Genovese2, Chelsea Canon3

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|May 9, 2014
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Genetic variants in Apolipoprotein L1 (APOL1) offer protection against African trypanosomes. These kidney disease-associated APOL1 variants mimic Old World monkey sequences, enhancing their ability to combat Trypanosoma brucei rhodesiense.

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Area of Science:

  • Genetics
  • Immunology
  • Parasitology

Background:

  • Apolipoprotein L1 (APOL1) confers protection against African trypanosomes in humans and primates.
  • Specific APOL1 genetic variants are strongly linked to kidney disease in African Americans.
  • These kidney risk variants exhibit enhanced trypanolytic activity against Trypanosoma brucei rhodesiense, the causative agent of acute sleeping sickness.

Purpose of the Study:

  • To investigate the coevolution between the APOL1 gene and trypanosomes using genetic, physiological, and biochemical approaches.
  • To understand the evolutionary origins of APOL1 kidney risk variants by analyzing sequences in humans and baboons and their geographic distribution.
  • To elucidate the molecular mechanism by which human trypanolytic APOL1 variants evade the Trypanosoma brucei rhodesiense virulence factor, serum resistance-associated protein (SRA).

Main Methods:

  • Analysis of APOL1 sequences in modern and archaic humans and baboons.
  • Assessment of geographic distribution of APOL1 variants in Africa.
  • In vivo testing of Old World monkey, human, and engineered APOL1 variants against human-infective trypanosomes.
  • Biochemical assays to determine SRA binding efficacy.

Main Results:

  • One APOL1 kidney risk variant, with a two-residue deletion, shifts a lysine residue mimicking Old World monkey sequences, enhancing trypanolytic activity by preventing SRA binding.
  • A second human APOL1 kidney risk allele, with an amino acid substitution, also aligns with Old World monkey sequences and shows reduced SRA binding, conferring protection against T. brucei rhodesiense.
  • Both APOL1 risk variants induced tissue injury in murine livers, indicating potential off-target effects.

Conclusions:

  • Human APOL1 kidney risk variants that protect against T. brucei rhodesiense have convergently evolved molecular signatures found in Old World monkeys.
  • The mechanism involves preventing SRA binding, thereby enhancing trypanolytic activity.
  • APOL1 variants may possess broader innate immune functions beyond trypanosome defense.