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PNAS 102 (44): 15791-15796

Copyright © 2005 by the National Academy of Sciences.

From The Cover


BIOCHEMISTRY

Dysregulation of TGF-{beta}1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice

Xiangchun Wang a b, Shinya Inoue a b, c, Jianguo Gu a, Eiji Miyoshi a, Katsuhisa Noda a, Wenzhe Li d, Yoko Mizuno-Horikawa a, Miyako Nakano a, Michio Asahi a, Motoko Takahashi a, e, Naofumi Uozumi a, Shinji Ihara a, Seung Ho Lee a, Yoshitaka Ikeda a, e, Yukihiro Yamaguchi a, f, Yoshiya Aze g, Yoshiaki Tomiyama c, Junichi Fujii a, h, Keiichiro Suzuki a, f, Akihiro Kondo d, Steven D. Shapiro i, Carlos Lopez-Otin j, Tomoyuki Kuwaki k, Masaru Okabe l, Koichi Honke a, m, and Naoyuki Taniguchi a, n

Departments of aBiochemistry, cInternal Medicine and Molecular Science, and dGlycotherapeutics, Osaka University Graduate School of Medicine, Osaka 565-0871, Japan; eDepartment of Cell Biology, Saga University School of Medicine, Saga 809-8501, Japan; fDepartment of Biochemistry, Hyogo College of Medicine, Hyogo 663-8501, Japan; gFukui Safety Institute, Ono Pharmaceutical Co., Fukui 913-8538, Japan; hDepartment of Biochemistry, Yamagata University School of Medicine, Yamagata 990-9585, Japan; iDepartment of Medicine, Section of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Boston, MA 02115; jDepartamento de Bioquimica y Biologia Molecular, Instituto Universitario de Oncologia, Universidad de Oviedo, 33006 Oviedo, Spain; kDepartment of Molecular and Integrative Physiology, Graduate School of Medicine, Chiba University, Chiba 260-8670, Japan; lDepartment of Experimental Genome Research, Genome Information Research Center, Osaka University, Osaka 565-0871, Japan; and mDepartment of Molecular Genetics, Kochi University Medical School, Kochi 783-8505, Japan

Communicated by David H. MacLennan, University of Toronto, Toronto, ON, Canada, August 24, 2005

Received for publication August 2, 2005.

Abstract: The core fucosylation ({alpha}1,6-fucosylation) of glycoproteins is widely distributed in mammalian tissues, and is altered under pathological conditions. To investigate physiological functions of the core fucose, we generated {alpha}1,6-fucosyltransferase (Fut8)-null mice and found that disruption of Fut8 induces severe growth retardation and death during postnatal development. Histopathological analysis revealed that Fut8-/- mice showed emphysema-like changes in the lung, verified by a physiological compliance analysis. Biochemical studies indicated that lungs from Fut8-/- mice exhibit a marked overexpression of matrix metalloproteinases (MMPs), such as MMP-12 and MMP-13, highly associated with lung-destructive phenotypes, and a down-regulation of extracellular matrix (ECM) proteins such as elastin, as well as retarded alveolar epithelia cell differentiation. These changes should be consistent with a deficiency in TGF-{beta}1 signaling, a pleiotropic factor that controls ECM homeostasis by down-regulating MMP expression and inducing ECM protein components. In fact, Fut8-/- mice have a marked dysregulation of TGF-{beta}1 receptor activation and signaling, as assessed by TGF-{beta}1 binding assays and Smad2 phosphorylation analysis. We also show that these TGF-{beta}1 receptor defects found in Fut8-/- cells can be rescued by reintroducing Fut8 into Fut8-/- cells. Furthermore, exogenous TGF-{beta}1 potentially rescued emphysema-like phenotype and concomitantly reduced MMP expression in Fut8-/- lung. We propose that the lack of core fucosylation of TGF-{beta}1 receptors is crucial for a developmental and progressive/destructive emphysema, suggesting that perturbation of this function could underlie certain cases of human emphysema.

Key Words: fucosylation • glycobiology • matrix metalloproteinase


Author contributions: X.W., J.G., E.M., and N.T. designed research; X.W., S. Inoue, K.N., W.L., Y.M.-H., M.N., N.U., S. Ihara, S.H.L., A.K., and T.K. performed research; X.W., S. Inoue, and M.O. contributed new reagents/analytic tools; X.W., J.G., M.A., M.T., Y.I., Y.Y., Y.A., Y.T., J.F., K.S., S.D.S., C.L.-O., and K.H. analyzed data; and X.W. and J.G. wrote the paper.

Freely available online through the PNAS open access option.

Abbreviations: ECM, extracellular matrix; MMP, matrix metalloproteinase; PA, 2-aminopyridine.

See Commentary on page 15721.

b X.W. and S. Inoue contributed equally to this work.

n To whom correspondence should be addressed at: Department of Biochemistry, Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan. E-mail: proftani{at}biochem.med.osaka-u.ac.jp.

© 2005 by The National Academy of Sciences of the USA


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