The Journal of Experimental Medicine
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Published 7 July 2003. doi:10.1084/jem.20021980
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© Rockefeller University Press, 0022-1007/2003/7/5 $5.00
The Journal of Experimental Medicine, Volume 198, Number 1, 5-17

Cellular Prion Protein Promotes Brucella Infection into Macrophages

Masahisa Watarai1, Suk Kim1, Janchivdorj Erdenebaatar1, Sou-ichi Makino1, Motohiro Horiuchi2, Toshikazu Shirahata1, Suehiro Sakaguchi3 and Shigeru Katamine3

1 Department of Applied Veterinary Science, Obihiro University of Agriculture and Veterinary Medicine, Hokkaido 080-8555, Japan
2 Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Hokkaido 080-8555, Japan
3 Department of Molecular Microbiology and Immunology, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki 852-8523, Japan

Address correspondence to Masahisa Watarai, Department of Applied Veterinary Science, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro-shi, Hokkaido 080-8555, Japan. Phone: 81-155-49-5387; Fax: 81-155-49-5386; E-mail: watarai{at}obihiro.ac.jp

The products of the Brucella abortus virB gene locus, which are highly similar to conjugative DNA transfer system, enable the bacterium to replicate within macrophage vacuoles. The replicative phagosome is thought to be established by the interaction of a substrate of the VirB complex with macrophages, although the substrate and its host cellular target have not yet been identified. We report here that Hsp60, a member of the GroEL family of chaperonins, of B. abortus is capable of interacting directly or indirectly with cellular prion protein (PrPC) on host cells. Aggregation of PrPC tail-like formation was observed during bacterial swimming internalization into macrophages and PrPC was selectively incorporated into macropinosomes containing B. abortus. Hsp60 reacted strongly with serum from human brucellosis patients and was exposed on the bacterial surface via a VirB complex–associated process. Under in vitro and in vivo conditions, Hsp60 of B. abortus bound to PrPC. Hsp60 of B. abortus, expressed on the surface of Lactococcus lactis, promoted the aggregation of PrPC but not PrPC tail formation on macrophages. The PrPC deficiency prevented swimming internalization and intracellular replication of B. abortus, with the result that phagosomes bearing the bacteria were targeted into the endocytic network. These results indicate that signal transduction induced by the interaction between bacterial Hsp60 and PrPC on macrophages contributes to the establishment of B. abortus infection.

Key Words: Hsp60 • type IV secretion • macropinocytosis • intracellular replication • brucellosis


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