Macrophages release neuraminidase and cleaved calreticulin for programmed cell removal

A Allison Banuelos (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) M Michelle Baez (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) A Allison Zhang (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) L Leyla Yılmaz (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) W William Kasberg (Department of Biomolecular Chemistry, School of Medicine and Public Health, University of Wisconsin) R Regan Volk (Department of Pharmaceutical Chemistry, Cardiovascular Research Institute, University of California) N Nardin Georgeos (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) E Elle Koren-Sedova (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) U Uyen Le (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) A Andrew T. Burden (Institute for Stem Cell Biology and Regenerative Medicine, School of Medicine, Stanford University) K Kristopher D. Marjon (Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine) J Jennifer Lippincott-Schwartz B Balyn W. Zaro (Department of Pharmaceutical Chemistry, Cardiovascular Research Institute, University of California) I Irving L. Weissman

Abstract

Calreticulin (CALR) is primarily an endoplasmic reticulum chaperone protein that also plays a key role in facilitating programmed cell removal (PrCR) by acting as an “eat-me” signal for macrophages, directing their recognition and engulfment of dying, diseased, or unwanted cells. Recent findings have demonstrated that macrophages can transfer their own CALR onto exposed asialoglycans on target cells, marking them for PrCR. Despite the critical role CALR plays in this process, the molecular mechanisms behind its secretion by macrophages and the formation of binding sites on target cells remain unclear. Our findings show that CALR undergoes C-terminal cleavage upon secretion, producing a truncated form that functions as the active eat-me signal detectable on target cells. We identify cathepsins as potential proteases involved in this cleavage process. Furthermore, we demonstrate that macrophages release neuraminidases, which modify the surface of target cells and facilitate CALR binding. These insights reveal a coordinated mechanism through which lipopolysaccharide (LPS)-activated macrophages regulate CALR cleavage and neuraminidase activity to mark target cells for PrCR. How they recognize the cells to be targeted remains unknown.

Article Details

Volume / Issue Vol. 122, Issue 21
Published May 27, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (14)

A

Allison Banuelos

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

M

Michelle Baez

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

A

Allison Zhang

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

L

Leyla Yılmaz

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

W

William Kasberg

Department of Biomolecular Chemistry, School of Medicine and Public Health, University of Wisconsin

R

Regan Volk

Department of Pharmaceutical Chemistry, Cardiovascular Research Institute, University of California

N

Nardin Georgeos

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

E

Elle Koren-Sedova

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

U

Uyen Le

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

A

Andrew T. Burden

Institute for Stem Cell Biology and Regenerative Medicine, School of Medicine, Stanford University

K

Kristopher D. Marjon

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine

J

Jennifer Lippincott-Schwartz

B

Balyn W. Zaro

Department of Pharmaceutical Chemistry, Cardiovascular Research Institute, University of California

I

Irving L. Weissman