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J. Biol. Chem., Vol. 283, Issue 27, 19039-19048, July 4, 2008

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Meichroacidin Containing the Membrane Occupation and Recognition Nexus Motif Is Essential for Spermatozoa Morphogenesis^*

Keizo Tokuhiro, Mika Hirose, Yasushi Miyagawa^¶, Akira Tsujimura^¶, Shinji Irie^||, Ayako Isotani, Masaru Okabe, Yoshiro Toyama^**, Chizuru Ito^**, Kiyotaka Toshimori^**, Ken Takeda, Shigeru Oshio, Hitoshi Tainaka, Junji Tsuchida¹, Akihiko Okuyama^¶, Yoshitake Nishimune, and Hiromitsu Tanaka²

From the TANAKA Project, Center for Advanced Science and Innovation, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Animal Resource Center for Infectious Diseases, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, the ^¶Department of Urology, Osaka University Graduate School of Medicine, 3-1 Yamadaoka, Suita, Osaka 565-0871, ^||Life Science Department, Business Incubation Center, Corporate Manufacturing, Technology, and Research Division, Toppan Printing Company, Ltd., 1-3-3 Suido, Bunkyo-ku, Tokyo 112-8531, the ^**Department of Anatomy and Developmental Biology, Graduate School of Medicine, Chiba University, Chiba 260-8670, the Department of Hygiene Chemistry, Faculty of Pharmaceutical Sciences, Tokyo University of Science, Chiba 278-8510, and Research Collaboration Center on Emerging and Re-emerging Infections, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan

Meichroacidin (MCA) is a highly hydrophilic protein that contains the membrane occupation and recognition nexus motif. MCA is expressed during the stages of spermatogenesis from pachytene spermatocytes to mature sperm development and is localized in the male meiotic metaphase chromosome and sperm flagellum. MCA sequences are highly conserved in Ciona intestinalis, Cyprinus carpio, and mammals. To investigate the physiological role of MCA, we generated MCA-disrupted mutant mice; homozygous MCA mutant males were infertile, but females were not. Sperm was rarely observed in the caput epididymidis of MCA mutant males. However, little to no difference was seen in testis mass between wild-type and mutant mice. During sperm morphogenesis, elongated spermatids had retarded flagellum formation and might increase phagocytosis by Sertoli cells. Immunohistochemical analysis revealed that MCA interacts with proteins located on the outer dense fibers of the flagellum. The testicular sperm of MCA mutant mice was capable of fertilizing eggs successfully via intracytoplasmic sperm injection and generated healthy progeny. Our results suggest that MCA is essential for sperm flagellum formation and the production of functional sperm.

Received for publication, October 16, 2007 , and in revised form, April 29, 2008.

^* This work was supported in part by grants received from Research and Development to Promote the Creation and Utilization of an Intellectual Infrastructure by the New Energy and Industrial Technology Development Organization of Japan and by the Ministry of Education, Culture, Sports, Science, and Technology of Japan. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1-S7 and Tables S1 and S2.

¹ Present address: Dept. of Patho-histocytochemistry, Discovery Research Technologies, Discovery Research Laboratories, Shionogi and Co., Ltd., Sagisu 5-12-4, Fukushima-ku, Osaka 553-0022, Japan.

² To whom correspondence should be addressed: Faculty of Pharmaceutical Sciences, Nagasaki International University, Huis Ten Bosch, Sasebo, Nagasaki 859-3298, Japan. Tel./Fax: 81-956-20-5651; E-mail: h-tanaka{at}niu.ac.jp.

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