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J. Biol. Chem., Vol. 279, Issue 20, 21421-21430, May 14, 2004

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Pulmonary Surfactant Protein A Augments the Phagocytosis of Streptococcus pneumoniae by Alveolar Macrophages through a Casein Kinase 2-dependent Increase of Cell Surface Localization of Scavenger Receptor A^*

Koji Kuronuma, Hitomi Sano¶, Kazunori Kato||, Kazumi Kudo, Naoki Hyakushima, Shin-ichi Yokota**, Hiroki Takahashi, Nobuhiro Fujii**, Hiroshi Suzuki, Tatsuhiko Kodama, Shosaku Abe, and Yoshio Kuroki¶¶¶

From the Department of Biochemistry, ^**Department of Microbiology, ^||Department of Molecular Medicine, and Third Department of Internal Medicine, Sapporo Medical University School of Medicine, Sapporo 060-8556, Japan, National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080-8555, Japan, Laboratory for Systems Biology and Medicine, Research Center for Advanced Science and Technology, University of Tokyo, Tokyo 153-8904, Japan, and ^¶CREST, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan

Pulmonary surfactant proteins A (SP-A) and D (SP-D), members of the collectin family, play important roles in the innate immune system of the lung. Here, we show that SP-A but not SP-D augmented phagocytosis of Streptococcus pneumoniae by alveolar macrophages, independent of its binding to the bacteria. Analysis of the SP-A/SP-D chimeras, in which progressively longer carboxyl-terminal regions of SP-A were replaced with the corresponding SP-D regions, has revealed that the SP-D region Gly³⁴⁶-Phe³⁵⁵ can be substituted for the SP-A region Leu²¹⁹-Phe²²⁸ without altering the SP-A activity of enhancing the phagocytosis and that the SP-A region Cys²⁰⁴-Cys²¹⁸ is required for the SP-A-mediated phagocytosis. Acetylated low density lipoprotein significantly reduced the SP-A-stimulated uptake of the bacteria. SP-A failed to enhance the phagocytosis of S. pneumoniae by alveolar macrophages derived from scavenger receptor A (SR-A)-deficient mice, demonstrating that SP-A augments SRA-mediated phagocytosis. Preincubation of macrophages with SP-A at 37 °C but not at 4 °C stimulated the phagocytosis. The SP-A-mediated enhanced phagocytosis was not inhibited by the presence of cycloheximide. SP-A increased cell surface localization of SR-A that was inhibitable by apigenin, a casein kinase 2 (CK2) inhibitor. SP-A-treated macrophages exhibited significantly greater binding of acetylated low density lipoprotein than nontreated cells. The SP-A-stimulated phagocytosis was also abolished by apigenin. In addition, SP-A stimulated CK2 activity. These results demonstrate that SP-A enhances the phagocytosis of S. pneumoniae by alveolar macrophages through a CK2-dependent increase of cell surface SR-A localization. This study reveals a novel mechanism of bacterial clearance by alveolar macrophages.

Received for publication, November 14, 2003 , and in revised form, February 11, 2004.

^* This work was supported in part by a grant-in-aid for scientific research from the Ministry of Education, Science, Sports and Culture, Japan and by the Akiyama Foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶¶ To whom correspondence should be addressed: Dept. of Biochemistry, Sapporo Medical University School of Medicine, Sapporo 060-8556, Japan. Tel.: 81-11-611-2111 (ext. 2670); Fax: 81-11-611-2236; E-mail: kurokiy{at}sapmed.ac.jp.

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