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© The Rockefeller University Press, 0021-9525/1999//527 $5.00
The Journal of Cell Biology, Volume 145, Number 3, , 1999 527-538

The Ligand for Osteoprotegerin (OPGL) Directly Activates Mature Osteoclasts

Teresa L. Burgess^*, Yi-xin Qian^*, Stephen Kaufman, Brian D. Ring, Gwyneth Van, Charles Capparelli, Michael Kelley, Hailing Hsu^||, William J. Boyle^||, Colin R. Dunstan, Sylvia Hu^*, and David L. Lacey

^* Department of Mammalian Cell Molecular Biology, Department of Pathology, Department of Protein Chemistry, and ^|| Department of Cell Biology, Amgen Inc., Thousand Oaks, California 91320-1789

Osteoprotegerin (OPG) and OPG-ligand (OPGL) potently inhibit and stimulate, respectively, osteoclast differentiation (Simonet, W.S., D.L. Lacey, C.R. Dunstan, M. Kelley, M.-S. Chang, R. Luethy, H.Q. Nguyen, S. Wooden, L. Bennett, T. Boone, et al. 1997. Cell. 89:309–319; Lacey, D.L., E. Timms, H.-L. Tan, M.J. Kelley, C.R. Dunstan, T. Burgess, R. Elliott, A. Colombero, G. Elliott, S. Scully, et al. 1998. Cell. 93: 165–176), but their effects on mature osteoclasts are not well understood. Using primary cultures of rat osteoclasts on bone slices, we find that OPGL causes approximately sevenfold increase in total bone surface erosion. By scanning electron microscopy, OPGL-treated osteoclasts generate more clusters of lacunae on bone suggesting that multiple, spatially associated cycles of resorption have occurred. However, the size of individual resorption events are unchanged by OPGL treatment. Mechanistically, OPGL binds specifically to mature OCs and rapidly (within 30 min) induces actin ring formation; a marked cytoskeletal rearrangement that necessarily precedes bone resorption. Furthermore, we show that antibodies raised against the OPGL receptor, RANK, also induce actin ring formation. OPGL-treated mice exhibit increases in blood ionized Ca⁺⁺ within 1 h after injections, consistent with immediate OC activation in vivo. Finally, we find that OPG blocks OPGL's effects on both actin ring formation and bone resorption. Together, these findings indicate that, in addition to their effects on OC precursors, OPGL and OPG have profound and direct effects on mature OCs and indicate that the OC receptor, RANK, mediates OPGL's effects.

Key Words: osteoclast • bone resorption • bone remodeling • osteoporosis • hematopoietic cell growth factors

Abbreviations used in this paper: MCSF/CSF-1, macrophage colony stimulating factor/colony stimulation factor-1; OC, osteoclasts; OPG/ OCIF, osteoprotegerin/osteoclast inhibitory factor; OPGL/ODF OPG, ligand/osteoclast differentiation factor (identical to RANKL and TRANCE); RANK, receptor activator of NF-B; RANKL, RANK ligand is identical to OPGL/ODF and TRANCE; TNF, tumor necrosis factor; TNFR, TNF receptor; TRANCE, TNF-related activation-induced cytokine is identical to OPGL/ODF; TRAF, TNFR-associated factor; TRAP, tartrate resistant acid phosphatase.

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