Stim1 Polymorphism Disrupts Immune Signaling and Creates Renal Injury in Hypertension

J Am Heart Assoc. 2020 Mar 3;9(5):e014142. doi: 10.1161/JAHA.119.014142. Epub 2020 Feb 20.

Abstract

Background Spontaneously hypertensive rats of the stroke-prone line (SHR-A3) develop hypertensive renal disease as a result of naturally occurring genetic variation. Our prior work identified a single-nucleotide polymorphism unique to SHR-A3 that results in truncation of the carboxy terminus of STIM1. The SHR-B2 line, which is also hypertensive but resists hypertensive renal injury, expresses the wild-type STIM1. STIM1 plays a central role in lymphocyte calcium signaling that directs immune effector responses. Here we show that major defects in lymphocyte function affecting calcium signaling, nuclear factor of activated T cells activation, cytokine production, proliferation, apoptosis, and regulatory T-cell development are present in SHR-A3 and attributable to STIM1. Methods and Results To assess the role of Stim1 variation in susceptibility to hypertensive renal injury, we created a Stim1 congenic line, SHR-A3(Stim1-B2), and STIM1 function was rescued in SHR-A3. We found that Stim1 gene rescue restores disturbed lymphocyte function in SHR-A3. Hypertensive renal injury was compared in SHR-A3 and the SHR-A3(Stim1-B2) congenic line. Histologically assessed renal injury was markedly reduced in SHR-A3(Stim1-B2), as were renal injury biomarker levels measured in urine. Stim1 deficiency has been linked to the emergence of antibody-mediated autoimmunity. Renal glomerular immunoglobulin deposition was greater in SHR-A3 than SHR-B2 and was reduced by Stim1 congenic substitution. Serum anti-double-stranded DNA antibody titers in SHR-A3 were elevated compared with SHR-B2 and were reduced in SHR-A3(Stim1-B2). Conclusions Stim1 deficiency in lymphocyte function originating from Stim1 truncation in SHR-A3 combines with hypertension to create end organ disease and may do so as a result of antibody formation.

Keywords: autoimmunity; hypertension; immunoglobulin; renal disease; spontaneously hypertensive rat.

Publication types

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

MeSH terms

  • Animals
  • Antibody-Dependent Cell Cytotoxicity
  • Autoimmunity
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism*
  • Calcium Signaling
  • Cells, Cultured
  • Disease Models, Animal
  • Hypertension / complications*
  • Hypertension / genetics
  • Hypertension / immunology
  • Hypertension / metabolism
  • Kidney / immunology
  • Kidney / metabolism*
  • Kidney / pathology
  • Kidney Diseases / etiology*
  • Kidney Diseases / genetics
  • Kidney Diseases / immunology
  • Kidney Diseases / metabolism
  • Lymphocyte Activation*
  • Male
  • NFATC Transcription Factors / metabolism
  • ORAI1 Protein / genetics
  • ORAI1 Protein / metabolism*
  • Polymorphism, Single Nucleotide*
  • Rats, Inbred SHR
  • Rats, Transgenic

Substances

  • NFATC Transcription Factors
  • ORAI1 Protein
  • Orai1 protein, rat