Loss of Siglec expression on T lymphocytes during human evolution

Proc Natl Acad Sci U S A. 2006 May 16;103(20):7765-70. doi: 10.1073/pnas.0510484103. Epub 2006 May 8.

Abstract

We report here that human T cells give much stronger proliferative responses to specific activation via the T cell receptor (TCR) than those from chimpanzees, our closest evolutionary relatives. Nonspecific activation using phytohemagglutinin was robust in chimpanzee T cells, indicating that the much lower response to TCR simulation is not due to any intrinsic inability to respond to an activating stimulus. CD33-related Siglecs are inhibitory signaling molecules expressed on most immune cells and are thought to down-regulate cellular activation pathways via cytosolic immunoreceptor tyrosine-based inhibitory motifs. Among human immune cells, T lymphocytes are a striking exception, expressing little to none of these molecules. In stark contrast, we find that T lymphocytes from chimpanzees as well as the other closely related "great apes" (bonobos, gorillas, and orangutans) express several CD33-related Siglecs on their surfaces. Thus, human-specific loss of T cell Siglec expression occurred after our last common ancestor with great apes, potentially resulting in an evolutionary difference with regard to inhibitory signaling. We confirmed this by studying Siglec-5, which is prominently expressed on chimpanzee lymphocytes, including CD4 T cells. Ab-mediated clearance of Siglec-5 from chimpanzee T cells enhanced TCR-mediated activation. Conversely, primary human T cells and Jurkat cells transfected with Siglec-5 become less responsive; i.e., they behave more like chimpanzee T cells. This human-specific loss of T cell Siglec expression associated with T cell hyperactivity may help explain the strikingly disparate prevalence and severity of T cell-mediated diseases such as AIDS and chronic active hepatitis between humans and chimpanzees.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD / immunology*
  • Antigens, Differentiation, Myelomonocytic / immunology*
  • B-Lymphocytes / cytology
  • B-Lymphocytes / immunology
  • Biological Evolution*
  • Calcium / metabolism
  • Cell Proliferation
  • Down-Regulation
  • Humans
  • Lectins / immunology*
  • Lymphocyte Activation
  • Pan troglodytes / immunology*
  • Receptors, Antigen, T-Cell / metabolism
  • Sialic Acids / metabolism
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology*

Substances

  • Antigens, CD
  • Antigens, Differentiation, Myelomonocytic
  • Lectins
  • Receptors, Antigen, T-Cell
  • SIGLEC5 protein, human
  • Sialic Acids
  • Calcium