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Originally published In Press as doi:10.1074/jbc.M107484200 on November 6, 2001

J. Biol. Chem., Vol. 277, Issue 2, 949-957, January 11, 2002
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Novel Cytoplasmic Proteins of Nontypeable Haemophilus influenzae Up-regulate Human MUC5AC Mucin Transcription via a Positive p38 Mitogen-activated Protein Kinase Pathway and a Negative Phosphoinositide 3-Kinase-Akt Pathway*

Beinan WangDagger §, David J. LimDagger , Jiahuai Han, Young S. Kim||, Carol B. Basbaum**, and Jian-Dong LiDagger §

From the Dagger  Gonda Department of Cell and Molecular Biology, House Ear Institute and the Department of Otolaryngology, University of Southern California, Los Angeles, California 90057, the  Department of Immunology, Scripps Research Institute, La Jolla, California 92037, and the || Gastrointestinal Research Laboratory, Veterans Affairs Medical Center and the ** Department of Anatomy, University of California, San Francisco, California 94143

Nontypeable Haemophilus influenzae (NTHi) is an important human pathogen that causes chronic otitis media with effusion (COME) in children and exacerbation of chronic obstructive pulmonary disease (COPD) in adults. Mucin overproduction, a hallmark of both diseases, has been shown to directly cause conductive hearing loss in COME and airway obstruction in COPD. The molecular mechanisms underlying mucin overproduction in NTHi infections still remain unclear. Here, we show that NTHi strongly up-regulates MUC5AC mucin transcription only after bacterial cell disruption. Maximal up-regulation is induced by heat-stable bacterial cytoplasmic proteins, whereas NTHi surface membrane proteins induce only moderate MUC5AC transcription. These results demonstrate an important role for cytoplasmic molecules from lysed bacteria in the pathogenesis of NTHi infections, and may well explain why many patients still have persistent symptoms such as middle ear effusion in COME after intensive antibiotic treatment. Furthermore, our results indicate that activation of p38 mitogen-activated protein kinase is required for NTHi-induced MUC5AC transcription, whereas activation of phosphoinositide 3-kinase-Akt pathway leads to down-regulation of NTHi-induced MUC5AC transcription via a negative cross-talk with p38 mitogen-activated protein kinase pathway. These studies may bring new insights into molecular pathogenesis of NTHi infections and lead to novel therapeutic intervention for COME and COPD.

* This work was supported by National Institutes of Health Grant RO1-DC04562 (to J.-D. L.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ To whom correspondence may be addressed: Gonda Dept. of Cell and Molecular Biology, House Ear Inst., 2100 W. Third St., Los Angeles, CA 90057. E-mail: jdli@hei.org or bwang{at}hei.org.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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