Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesoderm

Du, Aiping; Sanger, Jean M.; Linask, Kérsti K.; Sanger, Joseph W.

doi:10.1016/s0012-1606(03)00104-0

Cited by 97 publications

(157 citation statements)

References 39 publications

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“…This observation became one of the key elements of the model of myofibrillogenesis suggested by these authors (Du et al 2003;Sanger et al 2005). The fact that the initial stage of obscurin incorporation is associated with the formation of a narrow, gradually expanding space above the first-formed terminal Z-disc of each sarcomere agrees well with these data.…”

Section: Discussionsupporting

confidence: 78%

“…Four major hypotheses seeking to explain the mechanism of myofibril formation have been recently reviewed by Sanger et al (2005). These hypothetic models can be summarized as following: (1) template model that considers stress fiber-like structures as templates or scaffolds for assembly of myofibrils (Dlugosz et al 1984); (2) the "stitching" model in which the actin filaments and Z-bands assemble independently from myosin filaments (Schultheiss et al 1990;Holtzer et al 1997;Ojima et al 1999); (3) premyofibril model assuming the formation of premyofibrils as immediate structural precursors of myofibrils (Rhee et al 1994;Du et al 2003;Sanger 2005), and (4) direct assembly of myofibrils without any intermediate structures [for literature see Ehler et al (1999Ehler et al ( , 2004]. …”

Section: Introductionmentioning

confidence: 99%

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Early incorporation of obscurin into nascent sarcomeres: implication for myofibril assembly during cardiac myogenesis

Borisov

Martynova

Russell

2008

Histochem Cell Biol

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Obscurin is a recently identified giant multidomain muscle protein whose functions remain poorly understood. The goal of this study was to investigate the process of assembly of obscurin into nascent sarcomeres during the transition from non-striated myofibril precursors to striated structure of differentiating myofibrils in cell cultures of neonatal rat cardiac myocytes. Double immunofluorescent labeling and high resolution confocal microscopy demonstrated intense incorporation of obscurin in the areas of transition from non-striated to striated regions on the tips of developing myofibrils and at the sites of lateral fusion of nascent sarcomere bundles. We found that obscurin rapidly and precisely accumulated in the middle of the A-band regions of the terminal newly assembled half-sarcomeres in the zones of transition from the continuous, non-striated pattern of sarcomeric α-actinin distribution to cross-striated structure of laterally expanding nascent Z-discs. The striated pattern of obscurin typically ended at these points. This occurred before the assembly of morphologically differentiated terminal Z-discs of the assembling sarcomeres on the tips of growing myofibrils. The presence of obscurin in the areas of the terminal Z-discs of each new sarcomere was detected at the same time or shortly after complete assembly of sarcomeric structure. Many non-striated fibers with very low concentration of obscurin were already immunopositive for sarcomeric actin and myosin. This suggests that obscurin may serve for organization and alignment of myofilaments into the striated pattern. The comparison of obscurin and titin localization in these areas showed that obscurin assembly into the A-bands occurred soon after or concomitantly with incorporation of titin. Electron microscopy of growing myofibrils demonstrated intense formation and integration of myosin filaments into the "open" half-assembled sarcomeres in the areas of the terminal Z-I structures and at the lateral surfaces of newly formed, terminally located nascent sarcomeres. This process progressed before the assembly of the second-formed, terminal Z-discs of new sarcomeres and before the development of ultrastructurally detectable mature M-lines that define the completion of myofibril assembly, which supports the data of immunocytochemical study. Abundant non-aligned sarcomeres in immature myofibrils located on the growing tips were spatially separated and underwent the transition to the registered, aligned pattern. The sarcoplasmic reticulum, © Springer-Verlag 2008 aborisov@umich.edu. This paper is dedicated to the memory of Professor Pavel P. Rumyantsev (1927Rumyantsev ( -1988, a pioneer in studies of cardiac muscle differentiation, who is a lasting inspiration to all who worked with him. the organelle known to interact with obscurin, assembled around each new sarcomere. These results suggest that obscurin is directly involved in the proper positioning and alignment of myofilaments within nascent sarcomeres and in the establishment of the registered ...

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Section: Discussionsupporting

confidence: 78%

Section: Introductionmentioning

confidence: 99%

Early incorporation of obscurin into nascent sarcomeres: implication for myofibril assembly during cardiac myogenesis

Borisov

Martynova

Russell

2008

Histochem Cell Biol

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“…Previously, we demonstrated that NMHC-IIB is present during chick myocardial differentiation using precardiac mesoderm explant cultures to analyze myofibrillogenesis (Du et al, 2003). We, therefore, analyzed the possibility that NMHC-IIB may also be present in the directly loaded samples or in the flectin antibody immunoprecipitates, because the flectin antibody appeared to be recognizing a common epitope on the two isoforms (Fig.…”

Section: Nonmuscle Myosin-iib and -Iicmentioning

confidence: 99%

Cellular nonmuscle myosins NMHC‐IIA and NMHC‐IIB and vertebrate heart looping

Lu¹,

Seeholzer²,

Han³

et al. 2008

Developmental Dynamics

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Flectin, a protein previously described to be expressed in a left-dominant manner in the embryonic chick heart during looping, is a member of the nonmuscle myosin II (NMHC-II) protein class. During looping, both NMHC-IIA and NMHC-IIB are expressed in the mouse heart on embryonic day 9.5. The patterns of localization of NMHC-IIB, rather than NMHC-IIA in the mouse looping heart and in neural crest cells, are equivalent to what we reported previously for flectin. Expression of full-length human NMHC-IIA and -IIB in 10 T1/2 cells demonstrated that flectin antibody recognizes both isoforms. Electron microscopy revealed that flectin antibody localizes in short cardiomyocyte cell processes extending from the basal layer of the cardiomyocytes into the cardiac jelly. Flectin antibody also recognizes stress fibrils in the cardiac jelly in the mouse and chick heart; while NMHC-IIB antibody does not. Abnormally looping hearts of the Nodal ⌬ 600 homozygous mouse embryos show decreased NMHC-IIB expression on both the mRNA and protein levels. These results document the characterization of flectin and extend the importance of NMHC-II and the cytoskeletal actomyosin complex to the mammalian heart and cardiac looping. Developmental Dynamics 237:3577-3590, 2008.

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“…Further experiments will be required, however, to address whether the binding of some myosin isoforms (i.e., sarcomeric) to titin or M-line proteins is sufficient for sarcomeric integration, and whether or not this process is Ca 2ϩ -mediated. The data fit either of the two current myofibrillogenesis models: the premyofibril model in which myofibrils arise from precursor stress-fiberlike structures that contain both nonmuscle and muscle isoforms (Rhee et al, 1994;Dabiri et al, 1997;Du et al, 2003) and the independent model in which the major muscle myofilaments are synthesized independently and organize without reference to a preexisting myofibrillar template (Lu et al, 1992;Holtzer et al, 1997;Ehler et al, 1999;Rudy et al, 2001). However, the former model is supported by recent evidence that nonmuscle myosin IIB appears in a sarcomeric pattern before muscle myosin filaments during embryonic cardiac myofibrillogenesis, and blocking formation of these IIB filaments with the MLCK inhibitor ML-7 disrupts myofibrillogenesis (Du et al, 2003).…”

Section: Transients and Myofibrillogenesis Modelsmentioning

confidence: 86%

“…The data fit either of the two current myofibrillogenesis models: the premyofibril model in which myofibrils arise from precursor stress-fiberlike structures that contain both nonmuscle and muscle isoforms (Rhee et al, 1994;Dabiri et al, 1997;Du et al, 2003) and the independent model in which the major muscle myofilaments are synthesized independently and organize without reference to a preexisting myofibrillar template (Lu et al, 1992;Holtzer et al, 1997;Ehler et al, 1999;Rudy et al, 2001). However, the former model is supported by recent evidence that nonmuscle myosin IIB appears in a sarcomeric pattern before muscle myosin filaments during embryonic cardiac myofibrillogenesis, and blocking formation of these IIB filaments with the MLCK inhibitor ML-7 disrupts myofibrillogenesis (Du et al, 2003). This disruption phenocopies our results using ML-7 and other MLCK inhibitors on embryonic skeletal myocytes (Ferrari et al, 1998; this study), suggesting a conserved requirement for IIB or other nonmuscle myosin isoforms during cardiac and skeletal muscle myofibrillogenesis.…”

Section: Transients and Myofibrillogenesis Modelsmentioning

confidence: 86%

Calcium transients regulate patterned actin assembly during myofibrillogenesis

Cook

Terry

et al. 2003

Developmental Dynamics

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The highly ordered arrangement of sarcomeric myosin during striated muscle development requires spontaneous calcium (Ca 2ϩ ) transients. Here, we show that blocking transients also compromises patterned assembly of actin thin filaments, titin, and capZ. Because a conserved temporal assembly pattern has been described for these proteins, selective inhibitors of either thick or thin filament formation were used to determine their relative temporal interdependencies.

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Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesoderm

Cited by 97 publications

References 39 publications

Early incorporation of obscurin into nascent sarcomeres: implication for myofibril assembly during cardiac myogenesis

Early incorporation of obscurin into nascent sarcomeres: implication for myofibril assembly during cardiac myogenesis

Cellular nonmuscle myosins NMHC‐IIA and NMHC‐IIB and vertebrate heart looping

Calcium transients regulate patterned actin assembly during myofibrillogenesis

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