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Originally published In Press as doi:10.1074/jbc.M210712200 on January 27, 2003

J. Biol. Chem., Vol. 278, Issue 13, 11265-11272, March 28, 2003
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Phosphorylation or Glutamic Acid Substitution at Protein Kinase C Sites on Cardiac Troponin I Differentially Depress Myofilament Tension and Shortening Velocity*

Eileen M. BurkartDagger §, Marius P. SumandeaDagger , Tomoyoshi KobayashiDagger , Mahta Nili, Anne F. MartinDagger , Earl Homsher, and R. John SolaroDagger ||

From the Dagger  University of Illinois at Chicago, Department of Physiology and Biophysics, Program in Cardiovascular Sciences, College of Medicine, Chicago, Illinois 60612 and the  University of California at Los Angeles, Department of Physiology, School of Medicine, Center for Health Sciences, Los Angeles, California 90025

There is evidence that multi-site phosphorylation of cardiac troponin I (cTnI) by protein kinase C is important in both long- and short-term regulation of cardiac function. To determine the specific functional effects of these phosphorylation sites (Ser-43, Ser-45, and Thr-144), we measured tension and sliding speed of thin filaments in reconstituted preparations in which endogenous cTnI was replaced with cTnI phosphorylated by protein kinase C-epsilon or mutated to cTnI-S43E/S45E/T144E, cTnI-S43E/S45E, or cTnI-T144E. We used detergent-skinned mouse cardiac fiber bundles to measure changes in Ca2+-dependence of force. Compared with controls, fibers reconstituted with phosphorylated cTnI, cTnI-S43E/S45E/T144E, or cTnI-S43E/S45E were desensitized to Ca2+, and maximum tension was as much as 27% lower, whereas fibers reconstituted with cTnI-T144E showed no change. In the in vitro motility assay actin filaments regulated by troponin complexes containing phosphorylated cTnI or cTnI-S43E/S45E/T144E showed both a decrease in Ca2+ sensitivity and maximum sliding speed compared with controls, whereas filaments regulated by cTnI-S43E/S45E showed only decreased maximum sliding speed and filaments regulated by cTnI-T144E demonstrated only desensitization to Ca2+. Our results demonstrate novel site specificity of effects of PKC phosphorylation on cTnI function and emphasize the complexity of modulation of the actin-myosin interaction by specific changes in the thin filament.

* This work was supported by National Institutes of Health Grants R01 HL 64035 (Project 1, to R. J. S.), P01 HL 62426 (to R. J. S. and A. F. M.), RO1 AR-30988 (to E. H.), and T3207692 (to M. P. S. and E. M. B.), Individual National Research Service Award F32 HL 10409 (to M. P. S.), and American Heart Association Scientist Development Grant 0230038N (to T. K.).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.

§ Supported by an American Heart Association Pre-Doctoral Fellowship (Midwest Affiliate).

|| To whom correspondence should be addressed: Dept. of Physiology and Biophysics, (M/C 901), College of Medicine, University of Illinois at Chicago, 835 S. Wolcott Ave., Chicago, IL 60612-7342. Tel.: 312-996-7620; Fax: 312-996-1414; E-mail: SolaroRJ@uic.edu.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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