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Molecular and Cellular Biology, June 1999, p. 3969-3976, Vol. 19, No. 6
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Mid2 Is a Putative Sensor for Cell Integrity Signaling in Saccharomyces cerevisiae

Mathumathi Rajavel,1 Bevin Philip,1 Benjamin M. Buehrer,2 Beverly Errede,2 and David E. Levin1,*

Department of Biochemistry, School of Public Health, The Johns Hopkins University, Baltimore, Maryland 21205,1 and Department of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, North Carolina 275992

Received 19 January 1999/Returned for modification 10 February 1999/Accepted 4 March 1999

Hcs77 is a putative cell surface sensor for cell integrity signaling in Saccharomyces cerevisiae. Its loss of function results in cell lysis during growth at elevated temperatures (e.g., 39°C) and impaired signaling to the Mpk1 mitogen-activated protein kinase in response to mild heat shock. We isolated the MID2 gene as a dosage suppressor of the cell lysis defect of an hcs77 null mutant. MID2 encodes a putative membrane protein whose function is required for survival of pheromone treatment. Mid2 possesses properties similar to those of Hcs77, including a single transmembrane domain and a long region that is rich in seryl and threonyl residues. We demonstrate that Mid2 is required for cell integrity signaling in response to pheromone. Additionally, we show that Mid2 and Hcs77 serve a redundant but essential function as cell surface sensors for cell integrity signaling during vegetative growth. Both proteins are uniformly distributed through the plasma membrane and are highly O-mannosylated on their extracellular domains. Finally, we identified a yeast homolog of MID2, designated MTL1, which provides a partially redundant function with MID2 for cell integrity signaling during vegetative growth at elevated temperature but not for survival of pheromone treatment. We conclude that Hcs77 is dedicated to signaling cell wall stress during vegetative growth and that Mid2 participates in this signaling, but its primary role is in signaling wall stress during pheromone-induced morphogenesis.

* Corresponding author. Mailing address: Department of Biochemistry, The Johns Hopkins University, School of Public Health, 615 N. Wolfe St., Baltimore, MD 21205. Phone: (410) 955-9825. Fax: (410) 955-2926. E-mail: levin{at}welchlink.welch.jhu.edu.

Molecular and Cellular Biology, June 1999, p. 3969-3976, Vol. 19, No. 6
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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  • Martin, H., Rodriguez-Pachon, J. M., Ruiz, C., Nombela, C., Molina, M. (2000). Regulatory Mechanisms for Modulation of Signaling through the Cell Integrity Slt2-mediated Pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275: 1511-1519 [Abstract] [Full Text]  
  • Pruyne, D, Bretscher, A (2000). Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113: 365-375 [Abstract]  
  • Andrews, P., Stark, M. (2000). Type 1 protein phosphatase is required for maintenance of cell wall integrity, morphogenesis and cell cycle progression in Saccharomyces cerevisiae. J. Cell Sci. 113: 507-520 [Abstract]  
  • Mattison, C. P., Spencer, S. S., Kresge, K. A., Lee, J., Ota, I. M. (1999). Differential Regulation of the Cell Wall Integrity Mitogen-Activated Protein Kinase Pathway in Budding Yeast by the Protein Tyrosine Phosphatases Ptp2 and Ptp3. Mol. Cell. Biol. 19: 7651-7660 [Abstract] [Full Text]  
  • Delley, P.-A., Hall, M. N. (1999). Cell Wall Stress Depolarizes Cell Growth via Hyperactivation of Rho1. JCB 147: 163-174 [Abstract] [Full Text]  
  • Atienza, J. M., Suh, M., Xenarios, I., Landgraf, R., Colicelli, J. (2000). Human ERK1 Induces Filamentous Growth and Cell Wall Remodeling Pathways in Saccharomyces cerevisiae. J. Biol. Chem. 275: 20638-20646 [Abstract] [Full Text]  
  • Cabib, E., Roh, D.-H., Schmidt, M., Crotti, L. B., Varma, A. (2001). The Yeast Cell Wall and Septum as Paradigms of Cell Growth and Morphogenesis. J. Biol. Chem. 276: 19679-19682 [Full Text]  


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