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PubMed1991

Functional morphological interpretation of the distribution of muscle spindles in the jaw muscles of the mallard (Anas platyrhynchos).

The morphology and distribution of muscle spindles of jaw and tongue muscles in the mallard were examined in serial transverse sections of single muscles and in horizontal sections of a whole head. Our observations on spindle morphology are in agreement with previous descriptions of spindles in birds. Some spindles differ in their innervation and the pattern of intrafusal muscle fibers. The spindles of individual adductor and pterygoid muscles are distributed unevenly. Some adductor muscles lack spindles, whereas those of other muscles are confined to limited areas. Jaw opening muscles and extrinsic tongue muscles lack spindles. The stretch of extrafusal muscle fibers could be estimated from the difference in sarcomere length for birds with the beak open and closed. Not all muscle fiber groups are stretched evenly over the whole range of jaw opening. Only those fiber groups that are continuously stretched during jaw opening contain spindles.

Animals↗

PubMed2005

Asymmetric division of spindle microtubules and microfilaments during bovine meiosis from metaphase I to metaphase III.

The kinetics of spindle and chromosomes during bovine oocyte meiosis from meiosis I to meiosis III is described. The results of this study showed that (1) oocytes began to extrude the first polar body (Pb1) at the early anaphase I stage and the Pb1 totally separated from the mother cell only when oocytes reach the MII stage; (2) the morphology of the spindle changed from barrel-shaped at the metaphase stage to cylinder-shaped at early anaphase, and then to a thin, long triangle-shaped cone at late anaphase and telophase stages; (3) chromosome morphology went from an individual visible stage at metaphase to a less defined chromatin state during anaphase and telophase stages, and then back to visible individual chromosomes at the next metaphase; (4) chromatin that connected with the floor of the cone became the polar bodies and expelled, and almost all of the microtubules (MTs) and microfilaments (MFs) composing the spindles moved towards and contributed to the polar bodies; and (5) the size of the metaphase I (MI) spindle was larger than the metaphase II (MII) and metaphase III (MIII) spindles. The MII spindle, however, is more barrel-shaped than the MI spindle. This study suggests that spindle MTs and MFs during bovine oocyte meiosis are asymmetrically divided into the polar bodies.

Actin Cytoskeleton↗

PubMed2006

The fission yeast spindle orientation checkpoint: a model that generates tension?

In all eukaryotes, the alignment of the mitotic spindle with the axis of cell polarity is essential for accurate chromosome segregation as well as for the establishment of cell fate, and thus morphogenesis, during development. Studies in invertebrates, higher eukaryotes and yeast suggest that astral microtubules interact with the cell cortex to position the spindle. These microtubules are thought to impose pushing or pulling forces on the spindle poles to affect the rotation or movement of the spindle. In the fission yeast model, where cell division is symmetrical, spindle rotation is dependent on the interaction of astral microtubules with the cortical actin cytoskeleton. In these cells, a bub1-dependent mitotic checkpoint, the spindle orientation checkpoint (SOC), is activated when the spindles fail to align with the cell polarity axis. In this paper we review the mechanism that orientates the spindle during mitosis in fission yeast, and discuss the consequences of misorientation on metaphase progression.

Cell Division↗

PubMed1993

Ectopic spindle assembly during maturation of Xenopus oocytes: evidence for functional polarization of the oocyte cortex.

Inversion of stage VI Xenopus oocytes, when combined with cold-induced microtubule depolymerization, resulted in the displacement of the germinal vesicle (the oocyte nucleus) from its normal position in the animal hemisphere to a more equatorial or vegetal position. Confocal immunofluorescence microscopy with anti-tubulin antibodies revealed that the breakdown of ectopic germinal vesicles during progesterone-induced maturation of inverted oocytes was accompanied by the assembly of a transient MTOC-microtubule complex (MTOC-TMA complex) that migrated to the region of cortex nearest the site of GV breakdown. Formation of ectopic meiotic spindles, including spindle rotation and polar body formation, was observed with nearly equal frequency throughout the animal hemisphere. In contrast, the frequency of spindle formation in the vegetal hemisphere was substantially reduced. Many spindles that did form in more vegetal regions of the oocyte appeared unable to rotate and did not result in polar body formation. The results presented suggest that the assembly of meiotic spindles at the animal pole during maturation of Xenopus oocytes does not result from a specific targeting of the MTOC-TMA complex during oocyte maturation. However, the oocyte cortex does exhibit A-V polarization of its ability to support spindle rotation and polar body formation. Finally, the observed increase in the incidence of monaster formation in the vegetal hemisphere suggests that interactions between the nascent spindle and cortex may regulate spindle assembly and elongation.

Animals↗

PubMed1993

Okadaic acid affects spindle organization in metaphase II-arrested rat oocytes.

We used okadaic acid (OA), a potent phosphatase inhibitor, to study the role of phosphatases in the organization of the spindle microtubules in metaphase II-arrested rat oocytes. OA induced a dramatic elongation of the spindle and disorganization of the metaphase plate. Biochemical analysis revealed some dramatic changes after OA treatment: increased histone H1 kinase activity, a burst of protein phosphorylation, and inhibition of protein synthesis. The latter effect alone cannot be responsible for the changes in the spindle structure since inhibition of protein synthesis with puromycin had no such effect. To identify the targets of OA among the proteins associated with the spindle, meiotic spindles of OA-treated and control oocytes were purified. After OA treatment some proteins gained and others lost their association with the spindle. A few proteins that lost their affinity for the spindle also underwent hyperphosphorylation after OA treatment. These results suggest that hyperphosphorylation of some proteins associated with the spindle alters their affinity to microtubules and thus stabilizes them.

Animals↗

PubMed1991

Rat muscle spindle immunocytochemistry revisited.

The expression of myosin heavy chain isoforms in muscle spindle fibres has been the subject of a number of immunocytochemical studies, some of them with discordant results. In order to assess whether these discrepancies are due to differences in the specificity and sensitivity of the antibodies used, we have compared the reactivity of rat muscle spindle fibres to two pairs of antibodies presumed to be directed against slow tonic (ALD 19 and ALD 58) and neonatal (NN5) and neonatal/fast (MF30) myosin heavy chains. Adult, developing and neonatally de-efferented muscle spindles from the rat hind limb muscles were studied in serial cross-sections processed for the peroxidase-antiperoxidase method. Important differences in the staining profiles of intrafusal fibres were noted when ALD 19 and ALD 58 were compared. ALD 19 stained the muscle spindle precursors from the seventeenth day in utero, whereas ALD 58 only did so by the twentieth day of gestation. In adult spindles ALD 19 stained the nuclear bag1 fibres along their entire length, whereas ALD 58 did not stain these fibres towards their ends. ALD 19 stained the nuclear bag2 fibres along the A, B and inner C region, but ALD 58 stained these fibres only in the A and the inner B regions. ALD 19 stained some nuclear chain fibres along a short equatorial segment, whereas ALD 58 did not stain the nuclear chain fibres at all. NN5 stained the nascent nuclear bag1 and chain fibre precursors at earlier stages of development than MF30. Clear differential staining between primary and secondary generation of both extra- and intrafusal myotubes was seen with NN5, whereas MF30 stained all myotubes alike. However, in postnatal spindles, MF30 was a very good negative marker of nuclear bag1 fibres. The staining profile of the adult fibres with NN5 and MF30 was rather similar. The staining pattern of neonatally de-efferented bag fibres obtained with ALD 19 and ALD 58 was practically identical and it differed from that of control spindles, confirming that motor innervation participates in the regulation of the expression of slow tonic MHC along the length of the nuclear bag2 fibres, as we have previously shown with ALD 19. The distinct staining patterns obtained with ALD 19 versus ALD 58 and with NN5 versus MF30 reflect differences in antibody sensitivity and specificity. These differences account, in part, for the discrepancies in the results of previous studies on muscle spindles, published by Kucera and Walro using ALD 58 and MF30, and by us using ALD 19 and NN5.

Animals↗

PubMed1988

Motor and sensory innervation of muscle spindles in the neonatal rat.

Neural and muscular elements of three muscle spindles from the soleus muscles of 4-day-old rats were reconstructed by electron microscopy of skip-serial transverse ultrathin sections. Each spindle contained four encapsulated intrafusal fibers, including a minimum of one bag1, one bag2 and one chain fiber. The fibers were innervated by unmyelinated motor and sensory axons. The primary and secondary afferents approached the spindles as single axons and terminated on the central region of the intrafusal fibers. Single profiles of terminal axons occupied the sites of sensory neuromuscular junctions, similar to adult sensory endings. No morphological features suggested retraction of afferents from 4-day postnatal spindles. Motor axons approached spindles tightly packed in bundles of 5-20 axons and terminated in the juxtaequatorial and polar regions of both bag and chain fibers. Multiple profiles of terminal axons were visible for each intrafusal motor ending. More motor axons innervated 4-day postnatal spindles and a greater number of axon terminals were visible in immature intrafusal motor endings than in adult spindles. The data suggest that postnatal maturation of motor innervation to intrafusal fibers involves the elimination of supernumerary motor nerve inputs. Synapse elimination in the development of the fusimotor system might represent a mechanism whereby individual gamma axons adjust the number of spindles they innervate.

Animals↗

PubMed1989

Innervation of regenerated spindles in muscle grafts of the rat.

Features of the nerve supply and the encapsulated fibers of muscle spindles were assessed in grafted and normal extensor digitorum longus (EDL) muscles of rats by analysis of serial 10-microns frozen transverse sections stained for enzymes which delineated motor and sensory endings, oxidative capacity and muscle fiber type. The number of fibers was significantly more variable, and branched fibers were more frequently observed in regenerated spindles than in control spindles. Forty-eight percent of regenerated spindles received sensory innervation. Spindles reinnervated by afferents had a larger periaxial space than did spindles which were not reinnervated by afferents. Regenerated fibers innervated by afferents had small cross-sectional areas, equatorial regions with myofibrils restricted to the periphery of fibers, unpredictable patterns of nonuniform and nonreversible staining along the length of the fiber for 'myofibrillar' adenosine triphosphatase (mATPase) after acid and alkaline preincubation. In contrast, regenerated fibers devoid of sensory innervation resembled extrafusal fibers in that they usually exhibited myofibrils throughout the length of the fiber, no central aggregations of myonuclei, uniform staining for mATPase and a reversal of staining for mATPase after preincubation in an acid or alkaline medium. Approximately thirty percent of encapsulated fibers devoid of sensory innervation stained analogous to a type I extrafusal fiber, a pattern of staining never observed in intrafusal fibers of normal spindles. Groups of encapsulated fibers all exhibiting this pattern of staining reflect that either these fibers may have been innervated by collaterals of skeletomotor axons that originally innervated type I extrafusal fibers or that fibers innervated by only fusimotor neurons express patterns of staining for mATPase similar to extrafusal fibers in the absence of sensory innervation. Sensory innervation may also influence the reestablishment of multiple sites of motor endings on regenerated intrafusal fibers. Those regenerated fibers innervated by afferents had more motor endings than did regenerated fibers devoid of sensory innervation. Differences in size, morphology, and patterns of staining for mATPase and numbers of motor endings between fibers innervated by afferents and fibers devoid of sensory innervation reflect that afferents can influence the differentiation of muscle cells and the reestablishment of motor innervation other than during the late prenatal/early postnatal period when muscle spindles form and differentiate in rats.

Adenosine Triphosphatases↗

PubMed1984

Discharge activity of spindle afferents from the gastrocnemius-soleus muscle during head rotation in the decerebrate cat.

The activity of spindle afferents originating from both primary and secondary endings of the isometrically extended (6-8 mm) gastrocnemius-soleus (GS) muscle was recorded in precollicular decerebrate cats during sinusoidal head rotation about the longitudinal axis above a stationary body. In the first group of experiments to test the influence of vestibular volleys on fusimotor neurons, an acute bilateral neck deafferentation at C1-C3 was performed to eliminate possible influences arising from neck receptors; head rotation (0.026 Hz, +/- 15 degrees) induced a weak periodic rate modulation in 6/38 (15.8%) of the tested spindle afferents; the average response gain was 0.18 +/- 0.12, SD imp./s/deg (mean firing rate, 18.9 +/- 2.8 imp./s), and the average phase angle was -43.2 +/- 47.0 degrees, SD lag with respect to ipsilateral side-down displacement of the head (alpha-response pattern). In a second group of experiments head rotation studied after acute bilateral section of VIII cranial nerve, thereby stimulating only neck receptors, failed to influence in a reliable manner the firing rate of 38 additional spindle afferents. In a third group of experiments in which both VIII nerves and cervical dorsal roots were left intact, head rotation induced a response in 7/45 (15.6%) of the tested spindle afferents similar to that observed after cervical deafferentiation and thus depended on stimulation of labyrinth receptors alone. Over the examined frequency range of head rotation from 0.015 to 0.325 Hz (+/- 15 degrees), the response gain of spindle afferents was relatively stable during sinusoidal labyrinth stimulation. For most of the spindle afferents the phase angle of the response elicited at the lower frequencies was related to the direction of head orientation towards the ipsilateral sidedown, thus being attributed to labyrinth volleys originating from macular receptors; at 0325 Hz the stimulus was less effective and some units showed a phase advance relative to head position which was attributed to costimulation of canal receptors. Displacement of the muscle under study obtained by either rotation of the whole animal or body alone beneath a stationary head elicited a periodic modulation of spindle afferent discharge, independent of head orientation or type of preparation, in 51/73 (70%) of the muscle spindles tested; the average response gain was 0.20 +/- 0.19, SD imp./s/deg, and an average phase lead of +14.1 +/- 20.5 degrees, SD with respect to the peak of the ipsilateral side-down displacement of the body or of the animal was observed.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

PubMed2003

A novel yeast mutant that is defective in regulation of the Anaphase-Promoting Complex by the spindle damage checkpoint.

The accurate segregation of sister chromatids at the metaphase to anaphase transition in Saccharomyces cerevisiae is regulated by the activity of the anaphase-promoting complex or cyclosome (APC/C). In the event of spindle damage or monopolar spindle attachment, the spindle checkpoint is activated and inhibits APC/C activity towards the anaphase inhibitor Pds1p, resulting in a cell cycle arrest at metaphase. We have identified a novel allele of a gene for an APC/C subunit, cdc16-183, in S. cerevisiae. cdc16-183 mutants arrest at metaphase at 37 degrees C, and are supersensitive to the spindle-damaging agent nocodazole, which activates the spindle checkpoint, at lower temperatures. This supersensitivity to nocodazole cannot be explained by impairment of the spindle checkpoint pathway, as cells respond normally to spindle damage with a stable metaphase arrest and high levels of Pds1p. Despite showing metaphase arrest at G2/M at 37 degrees C, cdc16-183 mutants are able to perform tested G1 functions normally at this temperature. This is the first demonstration that a mutation in a core APC/C subunit can result in a MAD2-dependent arrest at the restrictive temperature. Our results suggest that the cdc16-183 mutant may have a novel APC/C defect(s) that mimics or activates the spindle checkpoint pathway.

Alleles↗

PubMed2005

Redundant mechanisms for anaphase chromosome movements: crane-fly spermatocyte spindles normally use actin filaments but also can function without them.

Actin inhibitors block or slow anaphase chromosome movements in crane-fly spermatocytes, but stopping of movement is only temporary; we assumed that cells adapt to loss of actin by switching to mechanism(s) involving only microtubules. To test this, we produced actin-filament-free spindles: we added latrunculin B during prometaphase, 9-80 min before anaphase, after which chromosomes generally moved normally during anaphase. We confirmed the absence of actin filaments by staining with fluorescent phalloidin and by showing that cytochalasin D had no effect on chromosome movement. Thus, actin filaments are involved in normal anaphase movements, but in vivo, spindles nonetheless can function normally without them. We tested whether chromosome movements in actin-filament-free spindles arise via microtubules by challenging such spindles with anti-myosin drugs. Y-27632 and BDM (2,3-butanedione monoxime), inhibitors that affect myosin at different regulatory levels, blocked chromosome movement in normal spindles and in actin-filament-free spindles. We tested whether BDM has side effects on microtubule motors. BDM had no effect on ciliary and sperm motility or on ATPase activity of isolated ciliary axonemes, and thus it does not directly block dynein. Nor does it block kinesin, assayed by a microtubule sliding assay. BDM could conceivably indirectly affect these microtubule motors, though it is unlikely that it would have the same side effect on the motors as Y-27632. Since BDM and Y-27632 both affect chromosome movement in the same way, it would seem that both affect spindle myosin; this suggests that spindle myosin interacts with kinetochore microtubules, either directly or via an intermediate component.

Actin Cytoskeleton↗

PubMed1985

Topographic studies relating distribution of Ia- and gamma-fibres in spinal cord and position of muscle spindles in cat tibialis anterior muscle.

The segmental distribution of 115 Ia- and 115 paired gamma-fibres of the tibialis anterior muscle was studied in anaesthetized cats. All Ia-fibres recorded were found in the lumbar segments L6 and L7, from caudal L6 to middle L7. The paired gamma-axons were also mainly found in these parts of the spinal cord, only 7 gamma-fibres were localized in caudal L7. A total of 70% of all fibres was found in L7. Of the fibres constituting 'muscle spindle units' of the tibialis anterior 92.2% enter the same segment (a 'muscle spindle unit' is here defined as a muscle spindle with its Ia-fibres and one gamma-fibre innervating it). More than that, 88% of the afferent and efferent fibres of muscle spindle units were found in the same part of the segment. For the first time, the position of the muscle spindles was related to the location of their Ia- and gamma-fibres in the spinal cord. In general, the muscle spindles located in the proximal muscle region project to the more cranial part of the spinal cord and the muscle spindles localized distally in the muscle project to the more caudal part of the spinal cord. The topographic pattern of the muscle spindle units is discussed with respect to the topographically arranged monosynaptic reflex loop.

Animals↗

PubMed1987

The role of tubulin polymerization during spindle elongation in vitro.

We describe the effect of exogenous tubulin on reactivation of anaphase spindle elongation in isolated diatom spindles. In the absence of tubulin, spindle elongation is limited to the equivalent of the microtubule overlap zone, but in the presence of tubulin spindle elongation is several times the length of the overlap zone. Biotinylated neurotubulin is incorporated into the overlap zone and around the poles. Before spindles have elongated by the equivalent of the overlap zone, there are two regions of incorporated tubulin flanking this zone. After further elongation, there is one broad zone of incorporated tubulin in the spindle midzone. Spindle elongation and the pattern of tubulin incorporation into the midzone, but not the poles, are ATP-dependent and vanadate-sensitive. These results suggest that tubulin adds onto the ends of microtubules in the overlap zone, which then slide through the midzone as the spindle elongates.

Adenosine Triphosphate↗

PubMed1990

Formation of the astral mitotic spindle: ultrastructural basis for the centrosome-kinetochore interaction.

The formation of the astral mitotic spindle is initiated at the time of nuclear envelope breakdown from an interaction between the replicated spindle poles (i.e. centrosomes) and the chromosomes. As a result of this interaction bundles of microtubules are generated which firmly attach the kinetochores on each chromosome to opposite spindle poles. Since these kinetochore fibers are also involved in moving the chromosomes, the mechanism by which they are formed is of paramount importance to understanding the etiology of force production within the spindle. As a prelude to outlining such a mechanism, the dynamics of spindle formation and chromosome behavior are examined in the living cell. Next, the properties of centrosomes and kinetochores are reviewed with particular emphasis on the structural and functional changes that occur within these organelles as the cell transits from interphase to mitosis. Finally, a number of recent observations relevant to the mechanism by which these organelles interact are detailed and discussed. From these diverse data it can be concluded that kinetochore fiber microtubules are derived from dynamically unstable astral microtubules that grow into, or grow by and then interact laterally with, the kinetochore. Moreover, the data clearly demonstrate that the interaction of a single astral microtubule with one of the kinetochores on an unattached chromosome is sufficient to attach the chromosome to the spindle, orient it towards a pole, and initiate poleward motion. As the chromosomes move into the region of the forming spindle more astral microtubules become incorporated into the nascent kinetochore fibers and chromosome velocity decreases dramatically. During this time the distribution of spindle microtubules changes from two overlapping radial arrays to the fusiform array characteristic of metaphase cells.

Animals↗

PubMed2006

The influence of pain on masseter spindle afferent discharge.

Muscle spindles provide proprioceptive feedback supporting normal patterns of motor activity and kinesthetic sensibility. During mastication, jaw muscle spindles play an important role in monitoring and regulating the chewing cycle and the bite forces generated during mastication. Both acute and chronic orofacial pain disorders are associated with changes in proprioceptive feedback and motor function. Experimental jaw muscle pain also alters the normal response of masseter spindle afferents to ramp and hold jaw movements. It has been proposed that altered motor function and proprioceptive input results from group III muscle afferent modulation of the fusimotor system which alters spindle afferent sensitivity in limb muscles. The response to nociceptive stimuli may enhance or reduce the response of spindle afferents to proprioceptive stimuli. Several experimental observations suggesting the possibility that a similar mechanism also functions in jaw muscles are presented in this report. First, evidence is provided to show that nociceptive stimulation of the masseter muscle primarily influences the amplitude sensitivity of spindle afferents with relatively little effect on the dynamic sensitivity. Second, reversible inactivation of the caudal trigeminal nuclei attenuates the nociceptive modulation of spindle afferents. Finally, functionally identified gamma-motoneurons in the trigeminal motor nucleus are modulated by intramuscular injection with algesic substances. Taken together, these results suggest that pain-induced modulation of spindle afferent responses are mediated by small diameter muscle afferents and that this modulation is dependent, in part, on the relay of muscle nociceptive information from trigeminal subnucleus caudalis onto trigeminal gamma-motoneurons. The implication of these results will be considered in light of current theories on the relationship between jaw muscle pain and oral motor function.

Afferent Pathways↗

PubMed2005

The effect of experimental muscle pain on the amplitude and velocity sensitivity of jaw closing muscle spindle afferents.

The effect of experimental muscle pain on the amplitude and velocity sensitivity of muscle spindle primary afferent neurons in the trigeminal mesencephalic nucleus (Vmes) was examined. Extracellular recordings were made from 45 neurons designated as spindle primary- or secondary-like on the basis of their response to ramp-and-hold jaw movements. Velocity sensitivity was assessed in spindle primary-like afferents by calculating the mean dynamic index of each unit in response to three different velocities of jaw opening before and after intramuscular injection with hypertonic saline (HS, 5%, 100 microl). The amplitude sensitivity of all jaw muscle spindle afferents was assessed by calculating the mean firing rate of each unit in response to three different amplitudes of jaw openings during both the open and hold phases of the movement and with best-fit lines obtained, using linear regression analysis, before and after HS injection. The variance of the two regression lines obtained for each unit before and after the injection was compared using the coincidence test, and changes in intercept and slope were determined. Seventy-five percent of the primary-like units and 80% of the secondary-like units presented with changes in static behavior after HS injection. Thirty-six percent of the primary-like units showed changes in dynamic behavior. Injection of isotonic saline (control) did not alter the responses of the spindle afferent to jaw opening. Thus, our results demonstrate that the predominant effect of noxious stimulation was a shift in the amplitude sensitivity of both spindle primary-like and secondary-like afferents and, to a lesser extent, the velocity sensitivity of the spindle primary-like unit. In accordance with earlier studies in the cat hindlimb and neck muscles, these results suggest that the activation of masseter muscle nociceptor alters spindle afferent responses to stretch acting primarily through static gamma motor neurons.

Animals↗

PubMed2004

Feo, the Drosophila homolog of PRC1, is required for central-spindle formation and cytokinesis.

We performed a functional analysis of fascetto (feo), a Drosophila gene that encodes a protein homologous to the Ase1p/PRC1/MAP65 conserved family of microtubule-associated proteins (MAPs). These MAPs are enriched at the spindle midzone in yeast and mammals and at the fragmoplast in plants, and are essential for the organization and function of these microtubule arrays. Here we show that the Feo protein is specifically enriched at the central-spindle midzone and that its depletion either by mutation or by RNAi results in aberrant central spindles. In Feo-depleted cells, late anaphases showed normal overlap of the antiparallel MTs at the cell equator, but telophases displayed thin MT bundles of uniform width instead of robust hourglass-shaped central spindles. These thin central spindles exhibited diffuse localizations of both the Pav and Asp proteins, suggesting that these spindles comprise improperly oriented MTs. Feo-depleted cells also displayed defects in the contractile apparatus that correlated with those in the central spindle; late anaphase cells formed regular contractile structures, but these structures did not constrict during telophase, leading to failures in cytokinesis. The phenotype of Feo-depleted telophases suggests that Feo interacts with the plus ends of central spindle MTs so as to maintain their precise interdigitation during anaphase-telophase MT elongation and antiparallel sliding.

Animals↗

PubMed2005

Modulation of muscle spindle innervation by neurotrophin-3 following nerve injury.

Muscle spindles monitor changes in muscle length and are innervated by groups Ia and II sensory axons as well as gamma motor axons. Ia sensory axons respond to neurotrophin-3 (NT-3), which plays an important role in sculpting proprioceptive development. Previously, transgenic mice were generated that overexpress NT-3 in muscle (mlc/NT-3 mice). These mice have alterations in proprioceptive elements due to the developmental actions of NT-3 and neuroprotective effects on Ia axons following nerve injury (Taylor, M.D., Vancura, R., Williams, J.M., Riekhof, J.T., Taylor, B.K., Wright, D.E., 2001. Overexpression of neurotrophin-3 in skeletal muscle alters normal and injury-induced limb control. Somatosens. Motor Res. 18 (4), 286-294.) Here, we investigated the actions of NT-3 on each class of injured axons innervating spindles and explored the mechanisms by which NT-3 acts. Immunohistochemical assessment of muscle spindle innervation following crush revealed that the degeneration of Ia axons innervating spindles in mlc/NT-3 mice was substantially reduced, and overall spindle innervation by group II and gamma fibers was greatly improved at later stages. Mlc/NT-3 mice also displayed a significant reduction in the expression of the injury-induced transcription factor ATF3 by retrogradely labeled muscle afferent neurons. The effects of transgenic NT-3 overexpression on spindle innervation could be mimicked if wild-type mice were treated intramuscularly with recombinant NT-3 prior to but not following injury, suggesting that NT-3's actions were due to preexposure to NT-3. This view was supported by in vitro experiments in which large DRG neurons from mlc/NT-3 mice grew significantly longer neurites than wild-type neurons. The results reveal that improved Ia-spindle interactions after injury may enhance spindle innervation by group II and gamma fibers. Finally, exposure of muscle afferent fibers to NT-3 prior to injury alters axonal responses both in vitro and in vivo.

Animals↗