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T-tubule formation in cardiacmyocytes: two possible mechanisms?

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Abstract

We have followed the differentiation of transverse (T) tubules and of the associations between sarcoplasmic reticulum (SR) and either the plasmalemma (peripheral couplings) or the T tubules (dyads) in postnatal rat ventricular myocytes using electron microscopy. Dyads and peripheral couplings are collectively called Ca2+ Release Units (CRUs) because they are the sites at which Ca2+ is released from the SR. Profiles of T tubules, caveolae and dyads are mostly at the cell edge in early postnatal days and are found with increased frequency in the cell interior during the first two postnatal weeks. Using ferritin to trace continuity of T tubules lumen with the extracellular space, we find that some of T tubules (between ∼6 and 25%), either singly or within dyads, lack ferritin in their lumen. The percentage of tubules that do not contain ferritin decreases slightly during postnatal differentiation and is not very different at the cells’ edges and interior. We propose that T tubules form as invaginations of the plasmalemma that penetrate inward driven by accrual of membrane lipids and specific proteins. This occurs by a dual mechanism: either by the independent flow of SR and T tubule proteins into the two separate membranes or by the fusion of preformed vesicle tandems into the dyads. Most of the CRUs (∼86%) are constituted by peripheral couplings and ferritin containing dyads, thus constituting CRUs in which Ca2+ release from the SR is initiated by a membrane depolarization. In the remaining CRUs, activation of Ca2+ release must be dependent on some other mechanisms.

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Acknowledgements

We would like to thank Ms. Nosta Glaser for her technical help during the experiments and Ms. Sara Marconi for her help in photography. This work was supported by NIH grant HL48093 (to C.F.A), HL-62571 (to R.M.A.) and by the American Heart Association grant-in-aid 0655656Z (to R.M.A.).

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Authors and Affiliations

  1. Department of Cell and Developmental Biology, School of Medicine, University of Pennsylvania, Anat/Chem Building, Room B42, Philadelphia, PA, 19104-6058, USA

    Alessandro Di Maio & Clara Franzini-Armstrong

  2. Department of Physiological Sciences, National Institute of Fitness and Sports Kanoya, Kagoshima, Japan

    Alessandro Di Maio

  3. Department of Physiology, Stritch School of Medicine, Loyola University Chicago, Maywood, IL, 60153, USA

    Kimberly Karko, Rose M. Snopko & Rafael Mejía-Alvarez

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  1. Alessandro Di Maio
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  2. Kimberly Karko
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  3. Rose M. Snopko
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  4. Rafael Mejía-Alvarez
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  5. Clara Franzini-Armstrong
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Correspondence to Alessandro Di Maio.

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Di Maio, A., Karko, K., Snopko, R.M. et al. T-tubule formation in cardiacmyocytes: two possible mechanisms?. J Muscle Res Cell Motil 28, 231–241 (2007). https://doi.org/10.1007/s10974-007-9121-x

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  • DOI: https://doi.org/10.1007/s10974-007-9121-x

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