Troponin and Titin Coordinately Regulate Length-dependent Activation in Skinned Porcine Ventricular Muscle

Terui, Takako; Sodnomtseren, Munguntsetseg; Matsuba, Douchi; Udaka, Jun; Ishiwata, Shin’ichi; Ohtsuki, Iwao; Kurihara, Satoshi; Fukuda, Norio

doi:10.1085/jgp.200709895

Cited by 48 publications

(110 citation statements)

References 41 publications

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“…Consistent with this view, varying the thin filament activation level by changing the concentration of MgADP [59] or inorganic phosphate (and H + ) [60] revealed that the length dependence is in proportion to the fraction of recruitable (i.e., resting) crossbridges that can potentially produce active force upon attachment to the thin filaments [61,62]. Recently, Terui et al [63] critically tested the idea that length-dependent activation is tuned via on-off switching of the thin filament state in concert with the titin-based regulations. It was demonstrated that the reconstitution of cardiac thin filaments with fast skeletal troponin (sTn) diminished length-dependent activation to a level similar to that observed in skeletal muscle, accompanied by the acceleration of crossbridge kinetics.…”

Section: The Role Of Titin In the Frank-starling Heart Mechanismmentioning

confidence: 78%

Physiological Functions of the Giant Elastic Protein Titin in Mammalian Striated Muscle

et al. 2008

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Abstract:The striated muscle sarcomere contains the third filament comprising the giant elastic protein titin, in addition to thick and thin filaments. Titin is the primary source of nonactomyosinbased passive force in both skeletal and cardiac muscles, within the physiological sarcomere length range. Titin's force repositions the thick filaments in the center of the sarcomere after contraction or stretch and thus maintains sarcomere length and structural integrity. In the heart, titin determines myocardial wall stiffness, thereby regulating ventricular filling. Recent studies have revealed the mechanisms involved in the fine tuning of titinbased passive force via alternative splicing or posttranslational modification. It has also been discovered that titin performs roles that go beyond passive force generation, such as a regulation of the Frank-Starling mechanism of the heart. In this review, we discuss how titin regulates passive and active properties of striated muscle during normal muscle function and during disease.

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Section: The Role Of Titin In the Frank-starling Heart Mechanismmentioning

confidence: 78%

Physiological Functions of the Giant Elastic Protein Titin in Mammalian Striated Muscle

et al. 2008

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“…In turn, reconstitution with cTn restored length-dependent activation and decreased Ca 2+ sensitivity. The authors associated the latter findings as an increased transition of the B-state towards the C-state (Terui et al 2008).…”

Section: Stretch Potentiates Titin-induced Strong-binding Cross-bridgmentioning

confidence: 97%

“…it mimics the effects of stretch), coincided with impaired lengthdependent activation (Smith and Fuchs 1999). Terui et al (2008) recently demonstrated that length-dependent activation is associated with titin-induced strain on the thick filament, which is highly dependent on the troponin complex. The authors observed that reconstitution of cardiac thin filaments with fast sTn reduced length-dependent activation to a level similar to that of skeletal muscle.…”

Section: Stretch Potentiates Titin-induced Strong-binding Cross-bridgmentioning

confidence: 98%

Historical perspective on heart function: the Frank–Starling Law

Sequeira

Velden

2015

Biophys Rev

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More than a century of research on the FrankStarling Law has significantly advanced our knowledge about the working heart. The Frank-Starling Law mandates that the heart is able to match cardiac ejection to the dynamic changes occurring in ventricular filling and thereby regulates ventricular contraction and ejection. Significant efforts have been attempted to identify a common fundamental basis for the Frank-Starling heart and, although a unifying idea has still to come forth, there is mounting evidence of a direct relationship between length changes in individual constituents (cardiomyocytes) and their sensitivity to Ca 2+ ions. As the Frank-Starling Law is a vital event for the healthy heart, it is of utmost importance to understand its mechanical basis in order to optimize and organize therapeutic strategies to rescue the failing human heart. The present review is a historic perspective on cardiac muscle function. We Brevive^a century of scientific research on the heart's fundamental protein constituents (contractile proteins), to their assemblies in the muscle (the sarcomeres), culminating in a thorough overview of the several synergistically events that compose the Frank-Starling mechanism. It is the authors' personal beliefs that much can be gained by understanding the Frank-Starling relationship at the cellular and whole organ level, so that we can finally, in this century, tackle the pathophysiologic mechanisms underlying heart failure.

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“…The mechanisms responsible are still debated, with evidence suggesting roles for Troponin C (Babu et al, 1988; but see , Troponin I (Arteaga et al, 2000), Titin (Fukuda et al, 2001;Fukuda et al, 2003;Terui et al, 2008), and lateral/radial spacing of the thick and thin filaments Williams et al, 2013).…”

Section: Fig 7 Predicted Muscle Lengthsmentioning

confidence: 99%

The length-force behavior and operating length range of squid muscle varies as a function of position in the mantle wall

Thompson

Shelton

Kier

2014

Journal of Experimental Biology

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Hollow cylindrical muscular organs are widespread in animals and are effective in providing support for locomotion and movement, yet are subject to significant non-uniformities in circumferential muscle strain. During contraction of the mantle of squid, the circular muscle fibers along the inner (lumen) surface of the mantle experience circumferential strains 1.3 to 1.6 times greater than fibers along the outer surface of the mantle. This transmural gradient of strain may require the circular muscle fibers near the inner and outer surfaces of the mantle to operate in different regions of the length-tension curve during a given mantle contraction cycle. We tested the hypothesis that circular muscle contractile properties vary transmurally in the mantle of the Atlantic longfin squid, Doryteuthis pealeii. We found that both the length-twitch force and length-tetanic force relationships of the obliquely striated, central mitochondria-poor (CMP) circular muscle fibers varied with radial position in the mantle wall. CMP circular fibers near the inner surface of the mantle produced higher force relative to maximum isometric tetanic force, P 0 , at all points along the ascending limb of the length-tension curve than CMP circular fibers near the outer surface of the mantle. The mean ± s.d. maximum isometric tetanic stresses at L 0 (the preparation length that produced the maximum isometric tetanic force) of 212±105 and 290±166 kN m −2 for the fibers from the outer and inner surfaces of the mantle, respectively, did not differ significantly (P=0.29). The mean twitch:tetanus ratios for the outer and inner preparations, 0.60±0.085 and 0.58±0.10, respectively, did not differ significantly (P=0.67). The circular fibers did not exhibit length-dependent changes in contraction kinetics when given a twitch stimulus. As the stimulation frequency increased, L 0 was approximately 1.06 times longer than L TW , the mean preparation length that yielded maximum isometric twitch force. Sonomicrometry experiments revealed that the CMP circular muscle fibers operated in vivo primarily along the ascending limb of the length-tension curve. The CMP fibers functioned routinely over muscle lengths at which force output ranged from only 85% to 40% of P 0 , and during escape jets from 100% to 30% of P 0 . Our work shows that the functional diversity of obliquely striated muscles is much greater than previously recognized.

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Troponin and Titin Coordinately Regulate Length-dependent Activation in Skinned Porcine Ventricular Muscle

Cited by 48 publications

References 41 publications

Physiological Functions of the Giant Elastic Protein Titin in Mammalian Striated Muscle

Physiological Functions of the Giant Elastic Protein Titin in Mammalian Striated Muscle

Historical perspective on heart function: the Frank–Starling Law

The length-force behavior and operating length range of squid muscle varies as a function of position in the mantle wall

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