Structural basis for oligomerization and glycosaminoglycan binding of CCL5 and CCL3

Liang, Wenguang G.; Triandafillou, Catherine G.; Huang, Teng-Yi; Zulueta, Medel Manuel L.; Banerjee, Shiladitya; Dinner, Aaron R.; Hung, Shang-Cheng; Tang, Wei-Jen

doi:10.1073/pnas.1523981113

Structural basis for oligomerization and glycosaminoglycan binding of CCL5 and CCL3

Journal Article · Mon Apr 18 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1523981113· OSTI ID:1254500

Liang, Wenguang G. ^[1]; Triandafillou, Catherine G. ^[1]; Huang, Teng-Yi ^[2]; Zulueta, Medel Manuel L. ^[2]; Banerjee, Shiladitya ^[1]; Dinner, Aaron R. ^[1]; Hung, Shang-Cheng ^[2]; Tang, Wei-Jen ^[1]

Univ. of Chicago, IL (United States)
Academia Sinica, Taipei (Taiwan)

CC chemokine ligand 5 (CCL5) and CCL3 are critical for immune surveillance and inflammation. Consequently, they are linked to the pathogenesis of many inflammatory conditions and are therapeutic targets. Oligomerization and glycosaminoglycan (GAG) binding of CCL5 and CCL3 are vital for the functions of these chemokines. Our structural and biophysical analyses of human CCL5 reveal that CCL5 oligomerization is a polymerization process in which CCL5 forms rod-shaped, double-helical oligomers. This CCL5 structure explains mutational data and offers a unified mechanism for CCL3, CCL4, and CCL5 assembly into high-molecular-weight, polydisperse oligomers. Here, a conserved, positively charged BBXB motif is key for the binding of CC chemokines to GAG. However, this motif is partially buried when CCL3, CCL4, and CCL5 are oligomerized; thus, the mechanism by which GAG binds these chemokine oligomers has been elusive. Our structures of GAG-bound CCL5 and CCL3 oligomers reveal that these chemokine oligomers have distinct GAG-binding mechanisms. The CCL5 oligomer uses another positively charged and fully exposed motif, KKWVR, in GAG binding. However, residues from two partially buried BBXB motifs along with other residues combine to form a GAG-binding groove in the CCL3 oligomer. The N termini of CC chemokines are shown to be involved in receptor binding and oligomerization. We also report an alternative CCL3 oligomer structure that reveals how conformational changes in CCL3 N termini profoundly alter its surface properties and dimer–dimer interactions to affect GAG binding and oligomerization. Such complexity in oligomerization and GAG binding enables intricate, physiologically relevant regulation of CC chemokine functions.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: NIH; National Science Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: W-31109-ENG-38

OSTI ID:: 1254500

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 18 Vol. 113; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
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CC chemokine
X-ray crystallography
glycosaminoglycan
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signal transduction

Structural basis for oligomerization and glycosaminoglycan binding of CCL5 and CCL3

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References (57)

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