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Infection and Immunity, March 2002, p. 1235-1244, Vol. 70, No. 3
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.3.1235-1244.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Recombinant Dirofilaria immitis Polyprotein That Stimulates Murine B Cells To Produce Nonspecific Polyclonal Immunoglobulin E Antibody

Hiroyuki Tezuka, Shinjiro Imai, Riho Muto, Yuko Furuhashi, and Koichiro Fujita^*

Section of Environmental Parasitology, Department of International Health Development, Division of Public Health, Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima Bunkyo-ku, Tokyo 113-8519, Japan

Received 4 June 2001/ Returned for modification 15 August 2001/ Accepted 29 November 2001

Nonspecific immunoglobulin E (IgE) production is an event characteristically observed in parasitic helminth infections, but its mechanisms are still unclear. To define these mechanisms, we prepared a recombinant Dirofilaria immitis protein (rDiAg) and assessed its effect on nonspecific IgE production. rDiAg preferentially induced nonspecific IgE production, without eliciting specific IgE production, as well as a Th2-type cytokine profile (high interleukin-4 [IL-4] and IL-10 production but low gamma interferon production) in BALB/c mice. rDiAg significantly elicited the proliferative response of naive B cells. This response was not abolished by polymyxin B, an inhibitor of lipopolysaccharide (LPS), and rDiAg normally expanded splenic B cells from LPS nonresponder C3H/HeJ mice. Thus, the mitogenic effect of rDiAg was not due to LPS contamination. rDiAg also enhanced levels of CD23 expression on splenic B cells. Splenic B cells produced marked levels of IgE when cultured with the combination of rDiAg and IL-4 (rDiAg-IL-4), whereas peritoneal B cells produced negligible levels of IgE. rDiAg-IL-4-induced IgE production by splenic B cells was synergistically increased by coculture with peritoneal B cells. rDiAg-driven IL-10 secretion was higher in peritoneal B cells than in splenic B cells. IgE production by splenic B cells cocultured with peritoneal B cells was decreased to a level comparable to that by splenic B cells in the presence of a neutralizing anti-IL-10 monoclonal antibody. Collectively, these results suggest that rDiAg-induced polyclonal expansion and IgE class switching of splenic B cells contribute to nonspecific IgE production and that these responses are enhanced by peritoneal B-cell-derived IL-10.

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* Corresponding author. Mailing address: Section of Environmental Parasitology, Department of International Health Development, Division of Public Health, Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima Bunkyo-ku, Tokyo 113-8519, Japan. Phone: 81-3-5803-5193. Fax: 81-3-5684-2849. E-mail: fuji.vip{at}0040tmd.ac.jp.

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Infection and Immunity, March 2002, p. 1235-1244, Vol. 70, No. 3
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.3.1235-1244.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

This article has been cited by other articles:

• Tezuka, H., Imai, S., Hidano, S., Tsukidate, S., Fujita, K. (2003). Various Types of Dirofilaria immitis Polyproteins Selectively Induce a Th2-Type Immune Response. Infect. Immun. 71: 3802-3811 [Abstract] [Full Text]  
• Tezuka, H., Imai, S., Tsukidate, S., Fujita, K. (2002). A Dirofilaria immitis Polyprotein Up-Regulates Nitric Oxide Production. Infect. Immun. 70: 5283-5286 [Abstract] [Full Text]