The Development of Extraocular Muscle Calcium Homeostasis Parallels Visuomotor System Maturation

Porter, John D.; Karathanasis, Paraskevi

doi:10.1006/bbrc.1999.0536

Cited by 16 publications

(11 citation statements)

References 33 publications

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“…Likewise, mitsugumin 29 (Mg29), a component of skeletal muscle triads, was reduced in EOM (Table 3). Although EOM expresses the known skeletal muscle SERCA1 and SERCA2 isoforms (31,32), SERCA1B (a neonatal isoform) and alternative isoforms of ryanodine receptor not represented on the Affymetrix array have been reported in fish EOM (33,34). We did observe a higher level of the sarcoplasmic reticulum calcium binding proteins, calsequestrin and cardiac calsequestrin, in EOM (Table 3).…”

Section: Transcription Factors and Cellmentioning

confidence: 60%

Extraocular muscle is defined by a fundamentally distinct gene expression profile

Porter

Khanna

Kaminski

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

204

198

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Skeletal muscle fibers are defined by patterned covariation of key traits that determine contractile and metabolic characteristics. Although the functional properties of most skeletal muscles result from their proportional content of a few conserved muscle fiber types, some, typically craniofacial, muscles exhibit fiber types that appear to lie outside the common phenotypic range. We analyzed gene expression profiles of three putative muscle classes, limb, masticatory, and extraocular muscle (EOM), in adult mice by high-density oligonucleotide arrays. Pairwise comparisons using conservative acceptance criteria identified expression differences in 287 genes between EOM and limb and͞or masticatory muscles. Use of significance analysis of microarrays methodology identified up to 400 genes as having an EOM-specific expression pattern. Genes differentially expressed in EOM reflect key aspects of muscle biology, including transcriptional regulation, sarcomeric organization, excitation-contraction coupling, intermediary metabolism, and immune response. These patterned differences in gene expression define EOM as a distinct muscle class and may explain the unique response of these muscles in neuromuscular diseases.

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Section: Transcription Factors and Cellmentioning

confidence: 60%

Extraocular muscle is defined by a fundamentally distinct gene expression profile

Porter

Khanna

Kaminski

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

204

198

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“…Their enhanced calcium handling capacities are believed to enable or assist these functions (Porter and Karathanasis, 1999; Andrade et al, 2005; Zeiger et al, 2010). Previous studies on EOMs have been limited to the examination of calcium transients in whole muscle (Andrade et al, 2005) or immature models (cultured myotubes, Zeiger et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…Total muscle Ca 2+ content is up to 40-fold higher in EOMs than in limb skeletal muscle (Porter and Karathanasis, 1999). Fast contracting muscles must be capable of rapid relaxation, and indeed, the key calcium pump (calcium ATPase, SERCA) is abundantly expressed in the sarcoplasmic reticulum (SR) of EOMs (Jacoby and Ko, 1993; Porter and Karathanasis, 1999). The extraordinarily fast contraction and relaxation of EOMs are correlated with the superior ability of EOMs to maintain calcium homeostasis (Khurana et al, 1995; Andrade et al, 2005; Zeiger et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Analysis of spontaneous and nerve-evoked calcium transients in intact extraocular muscles in vitro

Feng

Hennig

Corrigan

et al. 2012

Experimental Eye Research

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Extraocular muscles (EOMs) have unique calcium handling properties, yet little is known about the dynamics of calcium events underlying ultrafast and tonic contractions in myofibers of intact EOMs. Superior oblique EOMs of juvenile chickens were dissected with their nerve attached, maintained in oxygenated Krebs buffer, and loaded with fluo-4. Spontaneous and nerve stimulation-evoked calcium transients were recorded and, following calcium imaging, some EOMs were double-labeled with rhodamine-conjugated alpha-bungarotoxin (rhBTX) to identify EOM myofiber types. EOMs showed two main types of spontaneous calcium transients, one slow type (calcium waves with 1/2max duration of 2–12 s, velocity of 25–50 μm/s) and two fast “flash-like” types (Type 1, 30–90 ms; Type 2, 90–150 ms 1/2max duration). Single pulse nerve stimulation evoked fast calcium transients identical to the fast (Type 1) calcium transients. Calcium waves were accompanied by a local myofiber contraction that followed the calcium transient wavefront. The magnitude of calcium-wave induced myofiber contraction far exceeded those of movement induced by nerve stimulation and associated fast calcium transients. Tetrodotoxin eliminated nerve-evoked transients, but not spontaneous transients. Alpha-bungarotoxin eliminated both spontaneous and nerve-evoked fast calcium transients, but not calcium waves, and caffeine increased wave activity. Calcium waves were observed in myofibers lacking spontaneous or evoked fast transients, suggestive of multiply-innervated myofibers, and this was confirmed by double-labeling with rhBTX. We propose that the abundant spontaneous calcium transients and calcium waves with localized contractions that do not depend on innervation may contribute to intrinsic generation of tonic functions of EOMs.

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“…), was injected into postnatal day 56 (P56) mdx and wt mice (n=3 replicates/strain), as previously described (22). Mice were killed 20 h later, and cryostat sections were examined for myofiber dye incorporation.As an additional index of sarcolemmal integrity, total muscle Ca 2+ concentration was determined by atomic absorption spectroscopy (n=5 replicates/strain; 5 mice/replicate; P56) in mdx and wt mice, as previously described (23,24). Total muscle Ca 2+ content was expressed as mEq/kg of fat-free dry muscle.…”

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confidence: 99%

Constitutive properties, not molecular adaptations, mediate extraocular muscle sparing in dystrophicmdxmice

et al. 2003

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Extraocular muscle (EOM) is spared in Duchenne muscular dystrophy. Here, we tested putative EOM sparing mechanisms predicted from existing dystrophinopathy models. Data show that mdx mouse EOM contains dystrophin-glycoprotein complex (DGC)-competent and DGC-deficient myofibers distributed in a fiber type-specific pattern. Up-regulation of a dystrophin homologue, utrophin, mediates selective DGC retention. Counter to the DGC mechanical hypothesis, an intact DGC is not a precondition for EOM sarcolemmal integrity, and active adaptation at the level of calcium homeostasis is not mechanistic in protection. A partial, fiber type-specific retention of antiischemic nitric oxide to vascular smooth muscle signaling is not a factor in EOM sparing, because mice deficient in dystrophin and alpha-syntrophin, which localizes neuronal nitric oxide synthase to the sarcolemma, have normal EOMs. Moreover, an alternative transmembrane protein, alpha7beta1 integrin, does not appear to substitute for the DGC in EOM. Finally, genomewide expression profiling showed that EOM does not actively adapt to dystrophinopathy but identified candidate genes for the constitutive protection of mdx EOM. Taken together, data emphasize the conditional nature of dystrophinopathy and the potential importance of nonmechanical DGC roles and support the hypothesis that broad, constitutive structural cell signaling, and/or biochemical differences between EOM and other skeletal muscles are determinants of differential disease responsiveness.

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The Development of Extraocular Muscle Calcium Homeostasis Parallels Visuomotor System Maturation

Cited by 16 publications

References 33 publications

Extraocular muscle is defined by a fundamentally distinct gene expression profile

Extraocular muscle is defined by a fundamentally distinct gene expression profile

Analysis of spontaneous and nerve-evoked calcium transients in intact extraocular muscles in vitro

Constitutive properties, not molecular adaptations, mediate extraocular muscle sparing in dystrophicmdxmice

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