Transneuronal delivery of hyper-interleukin-6 enables functional recovery after severe spinal cord injury in mice methods
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Hyper-IL-6 promotes CST regeneration
Next, we tested whether AAV2-hIL-6 application, PTEN -/-, or their combination affect corticospinal tract (CST) regeneration following complete spinal cord crush (SCC). As AAV2 reaches higher neuronal transduction rates in newborn animals,, and to keep the methodology comparable to these previous studies, PTEN-floxed mice received injections of either AAV2-Cre (PTEN -/- ) or AAV2-GFP (PTEN +/+ ) into the left sensorimotor cortex at postnatal day 1 (P1). After 7 weeks, mice were subjected to SCC (Fig. ). Each received a second injection of either AAV2-hIL-6 or AAV2-GFP into the left sensorimotor cortex immediately afterward (Fig. ), resulting in four experimental groups: (a) Control animals that had received AAV2-GFP injections twice (PTEN +/+ ), (b) PTEN-floxed mice that were treated with AAV2-Cre and later with AAV2-GFP (PTEN -/&...
Hyper-IL-6 promotes functional recovery
Before tissue isolation and analysis, hindlimb movement had been analyzed in all four experimental groups using open-field locomotion tests according to the Basso Mouse Scale (BMS) over the postinjury period of 8 weeks. Consistent with previous reports -, the BMS score dropped down to 0 in all animals 1 day after injury, also indicating the completeness of the SCC (Fig. and Fig. ). Over time, control animals developed only active ankle movements, including spasms (Supplementary video ),, resulting in an average final score of 2 (Fig. and Fig. ). Despite the positive effect on CST-regeneration (Fig. ), PTEN -/- alone did not significantly improve the BMS score compared to AAV2-GFP treated controls (Fig. and Fig.; Supplementary video ). However, AAV2-hIL-6 treatment increased the BMS score to ∼4 by restor...
Cortical AAV2-hIL-6 delivery promotes RpST regeneration
The lack of functional recovery in PTEN -/- mice suggested that improved CST regeneration was not the leading cause for the AAV2-hIL-6 mediated functional recovery. As descending serotonergic (5-HT-positive) axons of the raphespinal tract (RpST) are reportedly relevant for locomotor recovery -, we stained and analyzed these axons in sagittal spinal cord sections of the same animals used in the previous experiments (Figs., ). Control (AAV2-GFP) and PTEN -/- mice only revealed sprouting of 5-HT-positive axons over distances of less than 1 mm beyond the crush site (Fig. and Fig. ). Remarkably, AAV2-hIL-6 treated mice showed more, and longer-distance regeneration of serotonergic fibers than controls or PTEN -/- (Fig. and Fig. ), with the longest axons reaching distances of >7 mm. Combinatorial treat...
AAV2-hIL-6-mediated recovery depends on the regeneration of serotonergic neurons
To investigate the relevance of RpST regeneration for functional recovery, adult mice of the same genetic background were subjected to SCC and received bilateral intracortical injections of either AAV2-hIL-6 or AAV2-GFP directly afterward (Fig. ). At week 6, when functional recovery in AAV2-hIL-6 treated mice had already reached maximal levels, the neurotoxin 5,7-dihydroxytryptamine (DHT) was intracerebroventricularly injected to selectively kill serotonergic neurons (Fig. ),,. The toxin almost completely abolished 5-HT positive neurons/axons in the medulla/spinal cord as soon as 1 day after injection (Fig. ). As described previously,,, other neurons remained unaffected, indicated by the successful BDA tracing of cortical motor neurons (Fig. ), presence of other neuN positive neurons next to depleted Raphe neurons in the medulla (Fig. ), and the alm...
AAV2-hIL-6 confers transneuronal stimulation of serotonergic fiber regeneration
We then investigated whether raphe neurons in the brain stem, which express the hIL-6 receptor GP130, receive synaptic input from transduced cortical motoneurons. To this end, we analyzed 5-HT stained brain stem tissue from mice 8 weeks after SCC and cortical AAV2-hIL-6 treatment as described above (Fig. ). GFP-positive sprouts of cortical motoneurons were located near 5-HT-positive raphe neurons in cross-sections of the medulla (Fig. ). The GFP signal and hIL-6 in the pyramidal axons were detected via high-resolution transversal scans after tissue clearing (Fig. ). Western blot analyses using brain stem lysates isolated 3 weeks after intracortical viral application showed pSTAT3 signals only in samples from AAV2-hIL-6-, but not AAV2-GFP-treated animals (Fig. and Fig. ), while total STAT3 protein expression or phosphorylation of eith...
AAV2-hIL-6 confers transneuronal stimulation of serotonergic fiber regeneration
To verify that cortical motoneurons were synaptically connected with raphe neurons, we used AAV1, which, in contrast to AAV2, can trans-synaptically transduce supraspinal target neurons. We injected AAV1-Cre into the left sensorimotor cortex of Rosa26-tdTomato (RFP) reporter mice and isolated their brain stem tissue after 2 weeks. RFP-positive (transduced) serotonergic neurons were detected in both sides of the nucleus raphe pallidus (NRPa) and the nucleus raphe magnus (NRM) (Fig. ) along their entire rostrocaudal length. Additionally, we performed a complementary experiment by injecting AAV1 directly into the raphe nuclei. As AAV1 is also retrogradely transported,, we found transduced neurons in the motor cortex layer V, confirming the synaptic connection to cortical neurons (Fig. ). Thus, cortically applied AAV2-hIL-6 transneuronally activates regenerative signal...
Methods
Male and female mice were used for all experiments. Wild-type C57BL/6 and 129/Ola mice were crossbred with PTEN f/f mice (C57BL/6;129) to obtain C57BL/6;129/J-TgH (Pten-flox) animals without further crossbreeding. C57BL/6J mice were obtained from Janvier Labs. Rosa26 loxP-stop-loxP-tdTomato (Rosa-tdTomato) mice were obtained from Jackson Laboratories (Stock No: 007914). All animals were housed under the same conditions for at least ten days before the start of experiments and generally maintained at 24 °C ambient temperature and 60% humidity with a 12 h light/dark cycle and ad libitum access to food and water. All experimental procedures were approved by the local animal care committee (LANUV Recklinghausen) and conducted in compliance with federal and state guidelines for animal experiments in Germany.
Intracortical injection of pups
Postnatal (P1) PTEN floxed (C57BL/6;129/J-TgH(Pten-flox)) pups were fixed on a stereotactic frame and continuously supplied with 2% isoflurane for anesthesia via a mouthpiece. A midline incision into the skin was made to expose the skull using microscissors. Since the skulls of P1 mice are still soft, the cortex could be accessed using a 30-gauge needle to create two small holes in the left skull hemisphere with the following coordinates: -0.2 mm and 0.3 mm anteroposterior, 1.0 mm lateral to bregma. For AAV2-GFP or AAV2-Cre application, 770 nl of the virus suspensions were injected at a depth of 0.5 mm into the two sites using a pulled glass pipette connected to a nanoliter injector (Nanoject II, Drummond). To inject 770 nl, we applied 11 pulses of 70 nl at a rate of 23 nl/s and waited for 10 s after each pulse to allow distr...
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Next, we tested whether AAV2-hIL-6 application, PTEN -/-, or their combination affect corticospinal tract (CST) regeneration following complete spinal cord crush (SCC). As AAV2 reaches higher neuronal transduction rates in newborn animals,, and to keep the methodology comparable to these previous studies, PTEN-floxed mice received injections of either AAV2-Cre (PTEN -/- ) or AAV2-GFP (PTEN +/+ ) into the left sensorimotor cortex at postnatal day 1 (P1). After 7 weeks, mice were subjected to SCC (Fig. ). Each received a second injection of either AAV2-hIL-6 or AAV2-GFP into the left sensorimotor cortex immediately afterward (Fig. ), resulting in four experimental groups: (a) Control animals that had received AAV2-GFP injections twice (PTEN +/+ ), (b) PTEN-floxed mice that were treated with AAV2-Cre and later with AAV2-GFP (PTEN -/- ), (c) mice that received AAV2-GFP and later, after SCC, AAV2-hIL-6 (hIL-6) and (d) mice that were treated with AAV2-Cre first and, after SCC, with AAV2-hIL-6 (PTEN -/- /hIL-6). Axonal biotinylated dextran amine (BDA)-tracing of the right CST (Fig. ) was performed 6 wee...
Before tissue isolation and analysis, hindlimb movement had been analyzed in all four experimental groups using open-field locomotion tests according to the Basso Mouse Scale (BMS) over the postinjury period of 8 weeks. Consistent with previous reports -, the BMS score dropped down to 0 in all animals 1 day after injury, also indicating the completeness of the SCC (Fig. and Fig. ). Over time, control animals developed only active ankle movements, including spasms (Supplementary video ),, resulting in an average final score of 2 (Fig. and Fig. ). Despite the positive effect on CST-regeneration (Fig. ), PTEN -/- alone did not significantly improve the BMS score compared to AAV2-GFP treated controls (Fig. and Fig.; Supplementary video ). However, AAV2-hIL-6 treatment increased the BMS score to ∼4 by restoring plantar stepping with full hindlimb weight support, followed by lift-off, forward limb advancement, and reestablishment of weight support at initial contact in most of the animals (Fig. and Fig.; Supplementary video ). Combinatorial treatment (PTEN -/- +R...
The lack of functional recovery in PTEN -/- mice suggested that improved CST regeneration was not the leading cause for the AAV2-hIL-6 mediated functional recovery. As descending serotonergic (5-HT-positive) axons of the raphespinal tract (RpST) are reportedly relevant for locomotor recovery -, we stained and analyzed these axons in sagittal spinal cord sections of the same animals used in the previous experiments (Figs., ). Control (AAV2-GFP) and PTEN -/- mice only revealed sprouting of 5-HT-positive axons over distances of less than 1 mm beyond the crush site (Fig. and Fig. ). Remarkably, AAV2-hIL-6 treated mice showed more, and longer-distance regeneration of serotonergic fibers than controls or PTEN -/- (Fig. and Fig. ), with the longest axons reaching distances of >7 mm. Combinatorial treatment of AAV2-hIL-6 and PTEN -/- had no additional effect (Fig. and Fig. ). Furthermore, as measured during functional recovery analysis (Fig. ), bilateral AAV2-hIL-6 treatment did not increase RpST regeneration further compared to a unilateral application of the virus (...
To investigate the relevance of RpST regeneration for functional recovery, adult mice of the same genetic background were subjected to SCC and received bilateral intracortical injections of either AAV2-hIL-6 or AAV2-GFP directly afterward (Fig. ). At week 6, when functional recovery in AAV2-hIL-6 treated mice had already reached maximal levels, the neurotoxin 5,7-dihydroxytryptamine (DHT) was intracerebroventricularly injected to selectively kill serotonergic neurons (Fig. ),,. The toxin almost completely abolished 5-HT positive neurons/axons in the medulla/spinal cord as soon as 1 day after injection (Fig. ). As described previously,,, other neurons remained unaffected, indicated by the successful BDA tracing of cortical motor neurons (Fig. ), presence of other neuN positive neurons next to depleted Raphe neurons in the medulla (Fig. ), and the almost normal open field movement in uninjured mice evaluated 1 week after DHT application (Fig. ). However, in injured animals, 1 day after DHT application, the BMS of AAV2-hIL-6-treated mice dropped down to similar levels as in AAV-GFP treated control animals, which themselves remained unaffect...
We then investigated whether raphe neurons in the brain stem, which express the hIL-6 receptor GP130, receive synaptic input from transduced cortical motoneurons. To this end, we analyzed 5-HT stained brain stem tissue from mice 8 weeks after SCC and cortical AAV2-hIL-6 treatment as described above (Fig. ). GFP-positive sprouts of cortical motoneurons were located near 5-HT-positive raphe neurons in cross-sections of the medulla (Fig. ). The GFP signal and hIL-6 in the pyramidal axons were detected via high-resolution transversal scans after tissue clearing (Fig. ). Western blot analyses using brain stem lysates isolated 3 weeks after intracortical viral application showed pSTAT3 signals only in samples from AAV2-hIL-6-, but not AAV2-GFP-treated animals (Fig. and Fig. ), while total STAT3 protein expression or phosphorylation of either AKT or S6 remained unchanged (Fig. and Figs., ). Additionally, transverse scans through cleared brain stem tissue (Fig., Supplementary video ) from hIL-6 treated animals, and immunostaining of coronal sections showed, on average, 46% ± 4.46 SEM of...
To verify that cortical motoneurons were synaptically connected with raphe neurons, we used AAV1, which, in contrast to AAV2, can trans-synaptically transduce supraspinal target neurons. We injected AAV1-Cre into the left sensorimotor cortex of Rosa26-tdTomato (RFP) reporter mice and isolated their brain stem tissue after 2 weeks. RFP-positive (transduced) serotonergic neurons were detected in both sides of the nucleus raphe pallidus (NRPa) and the nucleus raphe magnus (NRM) (Fig. ) along their entire rostrocaudal length. Additionally, we performed a complementary experiment by injecting AAV1 directly into the raphe nuclei. As AAV1 is also retrogradely transported,, we found transduced neurons in the motor cortex layer V, confirming the synaptic connection to cortical neurons (Fig. ). Thus, cortically applied AAV2-hIL-6 transneuronally activates regenerative signaling pathways in ipsi- and contralateral raphe neurons by releasing the protein at the axon terminals. Fig. 7 CST axon collaterals project to raphe nuclei. a Schematic illustration, indicating the cortical application, anterograde axonal transport, and terminal release of AAV1-Cre into raphe nuclei (...
Male and female mice were used for all experiments. Wild-type C57BL/6 and 129/Ola mice were crossbred with PTEN f/f mice (C57BL/6;129) to obtain C57BL/6;129/J-TgH (Pten-flox) animals without further crossbreeding. C57BL/6J mice were obtained from Janvier Labs. Rosa26 loxP-stop-loxP-tdTomato (Rosa-tdTomato) mice were obtained from Jackson Laboratories (Stock No: 007914). All animals were housed under the same conditions for at least ten days before the start of experiments and generally maintained at 24 °C ambient temperature and 60% humidity with a 12 h light/dark cycle and ad libitum access to food and water. All experimental procedures were approved by the local animal care committee (LANUV Recklinghausen) and conducted in compliance with federal and state guidelines for animal experiments in Germany.
Postnatal (P1) PTEN floxed (C57BL/6;129/J-TgH(Pten-flox)) pups were fixed on a stereotactic frame and continuously supplied with 2% isoflurane for anesthesia via a mouthpiece. A midline incision into the skin was made to expose the skull using microscissors. Since the skulls of P1 mice are still soft, the cortex could be accessed using a 30-gauge needle to create two small holes in the left skull hemisphere with the following coordinates: -0.2 mm and 0.3 mm anteroposterior, 1.0 mm lateral to bregma. For AAV2-GFP or AAV2-Cre application, 770 nl of the virus suspensions were injected at a depth of 0.5 mm into the two sites using a pulled glass pipette connected to a nanoliter injector (Nanoject II, Drummond). To inject 770 nl, we applied 11 pulses of 70 nl at a rate of 23 nl/s and waited for 10 s after each pulse to allow distribution of the virus solution. After injection, the pipette was left in place for 1 min before being carefully withdrawn, and the incision carefully closed with a 4-0 black silk suture.
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"datePublished": "2021",
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"identifier": "10.1038/s41467-020-20112-4"
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