Central Nervous System axonal regeneration by spatially targeted drug combinations

There are no known drugs or drug combinations that promote substantial central nervous system axonal regeneration after injury. We used systems pharmacology approaches to model pathways underlying axonal growth and identify a four-drug combination that regulates multiple subcellular processes in the cell body and axon using the optic nerve crush model in rats. We intravitreally injected agonists HU-210 (cannabinoid receptor-1) and IL-6 (interleukin 6 receptor) to stimulate retinal ganglion cells for axonal growth. We applied, in gel foam at the site of nerve injury, Taxol to stabilize growing microtubules, and activated protein C to clear the debris field since computational models predicted that this drug combination regulating two subcellular processes at the growth cone produces synergistic growth. Morphology experiments show that the four-drug combination promotes axonal regrowth to the optic chiasm and beyond. Physiologically, drug treatment restored pattern electroretinograms and some of the animals had detectable visual evoked potentials in the brain and behavioral optokinetic responses. We conclude that spatially targeted drug treatment can promote robust axonal regeneration and can restore limited functional recovery.

[1]  R. Iyengar,et al.  Extracellular histones, a new class of inhibitory molecules of CNS axonal regeneration , 2021, Brain communications.

[2]  D. Creel,et al.  Visually evoked potentials. , 2019, Handbook of clinical neurology.

[3]  A. Harvey,et al.  Optic nerve regeneration in mammals: Regenerated or spared axons? , 2017, Experimental Neurology.

[4]  J. Fawcett,et al.  Selective rab11 transport and the intrinsic regenerative ability of CNS axons , 2017, eLife.

[5]  R. Iyengar,et al.  Dynamic balance between vesicle transport and microtubule growth enables neurite growth , 2017 .

[6]  S. Goldman,et al.  3K3A–activated protein C stimulates postischemic neuronal repair by human neural stem cells in mice , 2016, Nature Medicine.

[7]  C. Passaglia,et al.  Retinal cross talk in the mammalian visual system. , 2016, Journal of neurophysiology.

[8]  Giovanni Coppola,et al.  A Systems-Level Analysis of the Peripheral Nerve Intrinsic Axonal Growth Program , 2016, Neuron.

[9]  J. Sanes,et al.  Restoration of Visual Function by Enhancing Conduction in Regenerated Axons , 2016, Cell.

[10]  Zhigang He,et al.  Intrinsic Control of Axon Regeneration , 2010, Neuron.

[11]  Jianwei Hou,et al.  Metallothionein-I/II Promotes Axonal Regeneration in the Central Nervous System* , 2015, The Journal of Biological Chemistry.

[12]  N. Renier,et al.  iDISCO: A Simple, Rapid Method to Immunolabel Large Tissue Samples for Volume Imaging , 2014, Cell.

[13]  C. Bandtlow,et al.  Peripheral Nerve Regeneration and NGF-Dependent Neurite Outgrowth of Adult Sensory Neurons Converge on STAT3 Phosphorylation Downstream of Neuropoietic Cytokine Receptor gp130 , 2014, The Journal of Neuroscience.

[14]  D. Baker,et al.  High-Resolution Microtubule Structures Reveal the Structural Transitions in αβ-Tubulin upon GTP Hydrolysis , 2014, Cell.

[15]  H. Willison,et al.  The pre‐synaptic motor nerve terminal as a site for antibody‐mediated neurotoxicity in autoimmune neuropathies and synaptopathies , 2014, Journal of anatomy.

[16]  Yasir Abdul,et al.  Preservation of retina ganglion cell function by morphine in a chronic ocular-hypertensive rat model. , 2012, Investigative ophthalmology & visual science.

[17]  Frank Bradke,et al.  Three-dimensional imaging of the unsectioned adult spinal cord to assess axon regeneration and glial responses after injury , 2011, Nature Medicine.

[18]  G. Feng,et al.  Sustained axon regeneration induced by co-deletion of PTEN and SOCS3 , 2011, Nature.

[19]  Frank Bradke,et al.  Microtubule Stabilization Reduces Scarring and Causes Axon Regeneration After Spinal Cord Injury , 2011, Science.

[20]  D. Fischer,et al.  Taxol Facilitates Axon Regeneration in the Mature CNS , 2011, The Journal of Neuroscience.

[21]  Ravi Iyengar,et al.  Cannabinoid 1 Receptor and Interleukin-6 Receptor Together Induce Integration of Protein Kinase and Transcription Factor Signaling to Trigger Neurite Outgrowth* , 2009, The Journal of Biological Chemistry.

[22]  L. Frishman,et al.  Retinal pathway origins of the pattern ERG of the mouse. , 2009, Experimental eye research.

[23]  Zhigang He,et al.  Promoting Axon Regeneration in the Adult CNS by Modulation of the PTEN/mTOR Pathway , 2008, Science.

[24]  Susana R. Neves,et al.  Design Logic of a Cannabinoid Receptor Signaling Network That Triggers Neurite Outgrowth , 2008, Science.

[25]  R. Schnaar,et al.  Gangliosides and Nogo Receptors Independently Mediate Myelin-associated Glycoprotein Inhibition of Neurite Outgrowth in Different Nerve Cells* , 2007, Journal of Biological Chemistry.

[26]  J. Griffin,et al.  The cytoprotective protein C pathway. , 2007, Blood.

[27]  James W. Fawcett,et al.  The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system , 2007, Brain Research Reviews.

[28]  R. B. Hart,et al.  The Cytokine Interleukin-6 Is Sufficient But Not Necessary to Mimic the Peripheral Conditioning Lesion Effect on Axonal Growth , 2006, The Journal of Neuroscience.

[29]  Prahlad T. Ram,et al.  The Gαo/i-coupled Cannabinoid Receptor-mediated Neurite Outgrowth Involves Rap Regulation of Src and Stat3* , 2005, Journal of Biological Chemistry.

[30]  M. Schwartz,et al.  Pattern electroretinography in a rat model of ocular hypertension: functional evidence for early detection of inner retinal damage. , 2005, Experimental eye research.

[31]  R M Douglas,et al.  Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system , 2005, Visual Neuroscience.

[32]  R. Iyengar,et al.  Cannabinoid Receptor-induced Neurite Outgrowth Is Mediated by Rap1 Activation through Gαo/i-triggered Proteasomal Degradation of Rap1GAPII* , 2005, Journal of Biological Chemistry.

[33]  M. Schwab,et al.  Inhibition of Nogo: A key strategy to increase regeneration, plasticity and functional recovery of the lesioned central nervous system , 2005, Annals of medicine.

[34]  M. Filbin,et al.  Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS , 2003, Nature Reviews Neuroscience.

[35]  L. Benowitz,et al.  Lens Injury Stimulates Axon Regeneration in the Mature Rat Optic Nerve , 2000, The Journal of Neuroscience.

[36]  Earl L. Smith,et al.  The photopic negative response of the macaque electroretinogram: reduction by experimental glaucoma. , 1999, Investigative ophthalmology & visual science.

[37]  R. Bradshaw,et al.  Induction of Neurite Outgrowth by Interleukin-6 Is Accompanied by Activation of Stat3 Signaling Pathway in a Variant PC12 Cell (E2) Line* , 1996, The Journal of Biological Chemistry.

[38]  M. Filbin,et al.  A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration , 1994, Neuron.

[39]  M. Fishman,et al.  GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  J. Povlishock,et al.  Pathobiology of traumatically induced axonal injury in animals and man. , 1993, Annals of emergency medicine.

[41]  Edwin Clarke,et al.  Cajal's Degeneration and regeneration of the nervous system , 1992, Medical History.

[42]  D. Spinelli,et al.  The ERG in response to alternating gratings in patients with diseases of the peripheral visual pathway. , 1981, Investigative ophthalmology & visual science.