FAQ #1: Will There Be A Cure For Spinal Cord Injury?

FAQ #1:  Will There Be A Cure for Spinal Cord Injury?
By Wise Young PhD MD, Rutgers University,
W. M. Keck Center for Collaborative Neuroscience
604 Allison Rd, Piscataway, NJ 08854-8082
First posted 22 December 2008

Will there be a cure for spinal cord injury?  This is the most frequently asked and often first question asked by people and families after spinal cord injury.  I answer yes to this question for the following reasons.

  • People and animals often recover substantially after “incomplete” spinal cord injury.  Animals can walk with only 5-10% of their axons [1].  A large majority (>90%) of people with even slight initial preservation of function at the lowest level of their spinal cord, i.e. anal sensation and sphincter control, recover ability to walk [2].  Examination of their spinal cords may indicate that they have only 10% of their spinal cord tracts remaining at the injury site.  The spinal cord is capable of tremendous plasticity.  Thus, depending on what the person has, regenerating and remyelinating even a small proportion of the axons in the spinal cord may be sufficient to restore substantial function to people with spinal cord injury.
  • The spinal cord can regenerate.  For over a century, scientists have reported that spinal cords of some animals and even mammals can regenerate under certain circumstances.  For example, lamprey [3], tadpoles [4], goldfish [5], and many other animals are able to regenerate their spinal cords.  For a long time, people thought that this was because these animals are evolutionarily primitive and that mammalian axons cannot regrow.  However, Aguayo, et al. [6-8] found that spinal axons can regrow in peripheral nerve but certain factors in the spinal cord inhibit growth [9].
  • Many therapies regenerate the spinal cords.  Over 100 individual therapies have been reported to stimulate axonal regeneration in the spinal cord. Please note that the following is by no means an exhaustive list of curative therapies of spinal cord injury.  I only cite representative recent publications supporting each therapy.  The point is that *many* therapies have been reported to regenerate the spinal cord.
    • Nogo and Nogo receptor blockers.  Nogo is a myelin-based protein that activates axonal receptors that act through rho and rho kinase to stop axonal growth.  Many ways of blocking Nogo or its receptors have been shown to increase regeneration:
      • Binding of Nogo with antibodies [10, 11] or soluble Nogo receptor protein [12]  stimulate regeneration.  The former is currently in clinical trial by Novartis.  The latter is being developed for clinical trial by Biogen.
      • Blocking Nogo receptor with a 66-amino acid fragment of Nogo [13].  The fragment apparently binds the nogo receptor and prevents further activation.
      • Blocking Lingo co-receptor also stimulates regeneration [14, 15].  .  Lingo is a co-receptor of the Nogo receptor.  This is being developed by Biogen.
      • Blocking rho kinase and rho (“rhok and rho”).  Rho kinase blockers stimulate regeneration in the spinal cord.  A modified version of a bacterial toxin that blocks rho, named Cethrin, has been reported to stimulate regeneration and functional recover in animals and in clinical trials  [23-27]
    • Chondroitinase.  The extracellular space contains glycoproteins that inhibit axonal growth.  These include chondroitin-6-sulfate proteoglycans (CSPG), which impedes axonal guidance and growth [28, 29].  Chondroitinase ABC is a bacterial enzyme that break down CSPG [30], allows regeneration [31, 32], and improves locomotor recovery [33].
    • Cyclic nucleotides.  Cyclic nucleotides convert neuronal growth cone responses from repulsion to attraction [34].  An increase in intracellular cAMP in axons will stimulate axons to grow and ignore growth inhibitors such as Nogo and CSPG [35, 36].   In zebrafish, where regeneration can occur but not of all neurons, cAMP application is helpful [37].  Several treatments are available to increase cAMP levels in neurons.  One is rolipram, a phosphodiesterase 4 (PDE4) inhibitor localized to the central nervous system.  Dibutyryl cAMP will enter the cells and directly increase cAMP.  The combination of Schwann cell transplant, rolipram, and dibutyryl-cAMP strongly stimulate regeneration [38, 39].
    • Combination Neurotrophins.  Several neurotrophins are known to stimulate regeneration in the spinal cord, even in the presence of growth inhibitors.  These include nerve growth factor (NGF), neurotrophin-3 (NT3), and glial-derived neurotrophic factor (GDNF).  Much evidence point to the importance of NT-3 [40-42] in combination with other factors [43-46].  BDNF may have undesirable effects [47].  A sustained source of these neurotrophins, however, is required for long-distance regeneration.   Fibroblast growth factor (FGF-2) [48] and FGF-1 [49] apparently improved regeneration.  This may be through stimulation of endogenous neural stem cells in the spinal cord [50].
    • Cellular Adhesion Molecules.  A number of cell adhesion molecules play a major role in axonal regeneration [51].  The most interesting one is L1, a member of the IgG superfamily of cell adhesion molecules, that bind to L1 expressed by other growing axons and stimulate the axons to grow in bundles, a process called fasciculation.  Increasing L1 expressing in the spinal cord stimulates regeneration [52].  Elimination of L1 reduces sensor fiber sprouting in mice [53] perhaps through manipulation of semaphorins [54].  Another regenerative CAM is N-CAM [55] but increasing CHL1 cellular adhesion may inhibit recovery [56].
    • Cell Transplants.  Many cell transplants have been reported to improve recovery after spinal cord injury
      • Olfactory Ensheathing Glia.  These cells are born in the nasal mucosa and migrate in the olfactory nerve to the olfactory bulb, facilitating growth and connection of olfactory axons.  The olfactory nerve is the only nerve in the body that continuously regenerates throughout adult life and its ability to do so is believe to be due to the presence of OEG cells.  These cells also express L1 and neurotrophins. Astrocytes do not respond to exposure to olfactory ensheathing glia with GFAP or CSPG secretion.  Transplantation of these cells improves recovery after spinal cord injury [57-69] and ventral root repair [70, 71], although one group suggests that Schwann cells may be better in a direct comparison [72, 73].
      • Umbilical cord blood mononuclear cells.  Several groups have reported the umbilical cord blood mononuclear cells, particularly CD34+ cells, stimulate regeneration and improve recovery in animals after spinal cord injury [74-79].  The mechanisms of action were not clear.   Human umbilical cord blood-derived CD34+ cells may attenuate spinal cord injury by stimulating vascular endothelial and other neurotrophic factors [80] and downregulated FAS [81]. Cord blood cells may even myelinated axons [82].  We recently found that cord blood mononuclear cells secrete neurotrophins and that lithium strongly boosts neurotrophin production by these cells.   One study suggest that myeloid cells are essential for peripheral nerve regeneration [83].  Cord blood cells are already being used for multiple neurological applications [84].
      • Mesenchymal stem cells.  These are pluripotent stem cells that can be isolated from bone marrow and other tissues.  Several groups have now reported that these cells are beneficial in spinal cord injury [85-87].   These cells may act through similar mechanisms as umbilical cord blood mononuclear cells production of neurotrophins and provision of a hospitable environment for axonal growth.  Mesenchymal cells can be isolated from human umbilical cord and have been reported to have beneficial effects in animal spinal cord injury models [88, 89] and stroke [90].  Carvalho, et al. [91], however, found that CD45+/CD34+ mesenchymal stem cells do not improve neurological recovery in Wistar rats after spinal cord contusion.
      • Astrocytes.  Several studies [92, 93] suggest that certain types of astrocytes facilitate regeneration in the spinal cord.  As opposed to astrocytes that react to injury and surround the injury site, these astrocytes provide a conducive pathway for axonal growth in the spinal cord [94]. Neural stem cells produce these astrocytes and this may account for beneficial effects of neural stem cell transplants into injured spinal cords.  Glial precursor cells likewise may be beneficial [95].
      • Neural stem cells.  These can be obtained from embryonic stem cells, aborted fetuses, or even autologous from the hippocampus or subventricular zones [96].  Many groups have suggested that these cells alone [97, 98], after differentiation [99] or genetic manipulation [100] or in combination with other cells such as olfactory ensheathing glia [101] or Schwann cells [41, 42] are beneficial for spinal cord injury.  One of the main questions that has not yet been answered is how will the transplanted cells interact with neural stem cells that may already be present in the spinal cord [102].
      • Oligodendroglial progenitor cells.  Many groups have transplanted oligodendroglial progenitor cells (O2A) to the spinal cord and have found significant improvement of function [103].  Whether this is due to the remyelination observed or regeneration of axons is not clear.  Keirstead, et al. [93-95] are planning to go to clinical trial with oligodendroglial progenitor cells derived from human embryonic stem cells with Geron.
    • Purine nucleotides.  Several purine nucleotides have been reported to stimulate regeneration of the spinal cord.  These include cGMP and adenosine [34] and the modified guanosine analog AIT-082 [104, 105].  The mechanism is not well understood but may be related to increased cAMP levels and other mechanisms described above.  Several groups have reported the beneficial effects of inosine on regeneration of the spinal cord [106].
    • Ephrins.  The ephrins are guidance molecules that play a role in telling axons whether they have grown into the right places in the central nervous system [107].  Injury upregulated certain ephrins and blockade of these ephrins stimulates regeneration in mammalian spinal cords [107-111].   In particular, EphA4 blocking peptide enhances corticospinal tract regeneration [112].  EphA4-deficient mice regenerate axons and show less astrocytic gliosis [113].
    • Biomaterials.  Many different biomaterials have been reported to support regeneration in spinal cord injury.  For example, self-assembling peptides form a scaffold that can be used to bridge injured rat spinal cords [114, 115] and inhibit glial scar formation and promote axonal elongation [116].  Many types of hydrogels [117-120], other gels [121], poly-lactic-coglycolic acid [122-124], poly-lactic acid [125-127], and other synthetic materials [128] have been tried.  Natural materials such chitosan [129], agarose [130, 131], and alginate [132] have been used.  Plasma, fibrin glue, laminin, and collagen are popular [133-138].  Many types of configurations have been used with and without embedded biological factors [139] or drugs [140].  Many invetigators seeded biomaterials with Schwann cells [141, 142], neural stem cells [143], bone marrow stromal cells [144].
    • Therapeutic vaccines.  Many investigators have vaccinated animals with various putative substances in the hopes of stimulating them to produce antibodies against axonal growth inhibitors, such as Nogo.  For example, Huang, et al. [145] immunized rats with their own spinal cords and found that this stimulated extensive regeneration of large numbers of corticospinal axons.  Vaccination with p472 (a peptide derived from Nogo A [146] and Nogo-66 [10] promotes axonal regeneration and motor recovery after spinal cord injury. DNA vaccination efficiently induces antibodies to Nogo-A without exacerbating experimental autoimmune encephalomyelitis [147, 148] and can stimulate retinal ganglion cell regeneration [149].  DNA vaccines of other known inhibitors, such a MAG and OMGP have been tried as well [150, 151].
    • Electrical Stimulation.  Many early studies suggest that electrical currents stimulate regeneration [152-160].  Electrical stimulation is often used to enhance regeneration and reinnervation by peripheral nerves [161, 162].  A recent clinical trial of oscillating currents [163] suggests improved function in humans [164].
    • Other Therapies.  Many other therapies have been reported to be beneficial for regeneration:
      • Artemin.  This factor promotes re-entry of multiple classes of sensory fiber into the spinal cord and re-establishment of synaptic function and behavior improvements [165].  Incidentally, olfactory ensheathing glia express artemin [166].
      • Erythropoietin.  This hematopoietic hormone is a potent inducer of immune system [167], is neuroprotective [168], reduces oxidative stress [169], enhances regeneration in the spinal cord [170], and has been reported to improve recovery after spinal cord injury[171].
      • Bone Morphogenetic Protein (BMP) inhibitors.  BMP’s are potent inhibitors of axons regeneration [107].  BMP-2/4 are elevated in oligodendroglial cells.  Intrathecal administration of Noggin, a soluble BMP antagonist, results in enhanced locomotor recovery and significant regrowth of the corticospinal tract after spinal cord contusion [172].  BMP, however, is used to treat glial-restricted precursor cells to create astrocytes that support axonal regeneration [93].
      • Methylprednisolone (MP).  While MP has long been regarded to be an inhibitor of axonal growth, if it is applied for too long, it apparently reduces CSPG expression by astrocytes and enhances axonal growth in injured spinal cord as a result [173].
      • Polysialic acid.  Induced expression of these molecules increased the number of axons growing into the lesion cavity by 20-fold [174].
      • Granulocyte colony-stimulating factor (G-CSF).  Pan, et al. [175] reported that G-CSF inhibits programmed cell death and stimulates neuronal progenitor differentiation, that the combination of G-CSF and neural stem cell transplants enhances regeneration in transected rat spinal cords.
  • Neuronal replacement therapies.  Injuries to the spinal cord, particularly to the cervical and lumbosacral enlargement, damage neurons.  When motoneurons are damaged, the muscles they innervate may undergo atrophy.  Most muscles are innervated by many motoneurons and therefore will survive even after severe injuries.  However, cauda equina and peripheral nerve injuries will eliminate all or most of the motor innervations of a muscle and cause the muscle to undergo atrophy.  Likewise, injuries to the conus may cause severe damage to sacral motor centers controlling bowel, bladder, and sexual functions.  In such situations, motoneuronal replacement may be required.  If you had asked me a decade ago whether neuronal replacement therapies were possible, I would have said that it was unlikely.  However, the discovery of stem cells has changed this situation considerably.
    • Neural stem cell transplants.  Scientists who receive their education more than a decade ago were taught that we were born with the neurons that we die with.  In other words, no new neurons are supposed to be created after birth.  This situation changed when many groups discovered that the brain and spinal cord contain neural stem cells that continue to make many thousands of neurons every day.  Therefore, replacement of neurons by endogenous neural stem cells is not only possible but also likely.
    • Embryonic stem cells.  Kerr, et al. [176, 177] has shown that neural stem cells derived from embryonic stem cells are able to replace motoneurons in the spinal cord of animals that have had viral induced motoneuronal death.  When the cell transplants were combined with some of regenerative therapies described above, the neurons not only received input from descending tracts but grew their axons out of ventral roots to re-innervate muscle.   However, some researchers have found that embryonic stem cells do not replace neurons [178].
    • Stimulation of endogenous stem cells.  Lithium drug has long been used to treat manic depression.  Recent studies suggest that this drug may be acting through stimulation of endogenous neural stem cells [179], stimulates spinal cord regeneration [180, 181], supports retinal ganglion survival and axon regeneration [182], and may even reduce neuropathic pain [183].  A recent study [184, 185] suggests that this drug remarkably stops progression of amyotrophic lateral sclerosis.  Although the mechanisms are not well understood, one possible mechanism is through stimulation of endogenous neural stem cells in the spinal cord.
  • Many therapies stimulate remyelination of spinal axons.  Trauma damages not only axons and neurons but also oligodendroglia responsible for myelinating axons in the spinal cord.  Remyelination decreases with age [186].  In addition, oligodendroglia undergo apoptosis in the spinal cord when exposed to pro-inflammatory cytokines such as tumor necrosis factor alpha (TNF-alpha).  Furthermore, regenerating axons are naked and need to be myelinated in order to function optimally.  Fortunately, many therapies remyelinate the spinal cord.
    • Oligodendroglial progenitors.  These are cells that make oligodendroglia and can be derived from embryonic stem cells or neural stem cells.  Many investigators have shown that these cells will remyelinate the spinal cord [187]. Geron is planning a clinical trial to assess the effects of pre-differentiated oligodendroglia progenitor cells derived from human embryonic stem cells [188].
    • Schwann cells.  These are of course the cells that myelinate peripheral axons.  Schwann cells sometimes invade into the spinal cord injury site and, when they do invade, will remyelinate most of the spinal axons.   Transplanted Schwann cells were the first transplanted cells to remyelinate axons of the central nervous system [189].  The Schwann cells can also be genetically modified to express molecules that facilitate myelination [55].   However, they have been reported to be non-contributory to regeneration [190].
    • Olfactory ensheathing glia.  In addition to facilitating regeneration [191], OEG cells not only stimulate myelination [192, 193] but themselves can myelinate axons [194, 195] like Schwann cells. These cells can be obtained from adult olfactory bulb and nasal mucosa [196] and fetal olfactory bulb.  The first would be autografts and the latter would be heterografts.
    • Mesenchymal stem cells.  These have been reported to stimulate remyelination in rats [197].  Likewise, bone marrow cells have been reported to stimulate remyelination of the spinal cord [85, 198-201].
    • Myelination antibodies.  Several IgM antibodies have been reported to stimulate remyelination in the spinal cord.  The mechanism is not well understood but these antibodies appear to working as signalling antibodies that stimulate remyelination to occur in the spinal cord [202-204].
  • Combination therapies are necessary for significant regeneration.  It has become clear that combination therapies are necessary for the cure of spinal cord injury.  No single therapy can address all the obstacles to regeneration and neuronal replacement in the spinal cord.  In order for rivers of axons to cross the spinal cord injury site, therapies will need to address at least three obstacles:
    • Bridge the injury site.  Shortly after injury, the injury site is often filled with inflammatory cells and is bereft of cellular adhesion molecules that may help guide and facilitate axonal growth.  In chronic spinal cord injury, the injury site is often walled off by astrocytes that may consider the injury site to be “outside” of the central nervous system.  The extracellular matrix may be filled with CSPG.  To get around this, it is often useful to transplant cells that can “bridge” the gap and allow axons to growth through the injury site.  Many cells can serve this purpose, including astrocytes, olfactory ensheathing glia, umbilical cord blood mononuclear cells, mesenchymal stem cells, and others.
    • Sustained source of growth factors.  Axonal regeneration is very slow, probably no faster than a millimeter per day.  Therefore, a source of sustained growth factor is necessary for long-distance and long-term growth.  These include cells that secrete neurotrophins and a means of stimulating them to do so for long periods.  We recently discovered that lithium stimulates umbilical cord blood mononuclear cells to secrete three of the most important neurotrophins and therefore have proposed a clinical trial to test the effects of combination umbilical cord blood mononuclear cell transplants and lithium.
    • Block growth inhibitors.  At least two known proteins are known to inhibit axonal growth in the spinal cord.  The first is Nogo and several therapies are known to block Nogo, including antibodies against Nogo, Nogo receptor blockers, and blockers of rho [26] or rho kinase that mediate the effects of Nogo.  The second is CSPG and chondroitinase is known to break down CSPG and allow regeneration.  An alternative is a molecule called decorin, which inhibits CSPG production and may allow axonal growth to occur in chronic spinal cord injury [205, 206].

One legitimate question that might be asked is why we don’t have a cure for spinal cord injury already, given all these treatments that regenerate and remyelinate the spinal cords of animals?  Scientists design their experiments to show the possibilities of therapies, choosing models and outcome measures that maximally reflect the benefits of the therapies.  In the clinical situation, different obstacles to regeneration and recovery may be present, such as learned non-use, atrophy, spasticity, and pain.  Of course, animals aren’t being told by their doctors that they won’t walk.  They keep trying.  Animal models of spinal cord differ from the human situation in one important respect.  The distances that axons have to regrow in a rat are much shorter than those in the human.  Finally, few of these therapies have been tried in clinical trials.  When they have been applied, it is often in situations that mitigated against showing the therapeutic efficacy, e.g. using cells that are not immune-matched for transplantation, not addressing all the obstacles to regeneration, not including rehabilitation in the clinical trial protocol, and not providing credible documentation of patient recovery.

In summary, there are many reasons to be optimistic that there will be not just one but many “cures” for spinal cord injury.  I defined a cure as a treatment that would make it so that an observer who did not know you wouldn’t be able to tell that you have spinal cord injury.  I believe that there will be a cure because much data indicate that the spinal cord can regenerate and many therapies restore function in animal studies.  One or more of these will be shown to be successful in people in the coming years, hopefully sooner rather than later.  At the present, we don’t have the clinical trial infrastructure to test all the therapies that have shown promise in animal models.  It is likely that some combination of the therapies will provide cures.  However, we must be aware that the translation of findings from animal studies to human clinical trials will not necessarily be smooth and there will be bumps along the way.

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3 Responses to “FAQ #1: Will There Be A Cure For Spinal Cord Injury?”

  1. Simon Roulstone Says:

    Great article Wise, really interesting, and a great insight into what will hopefully develop in the future to reverse this devastating condition.

    Best regards

    Simon
    C5/6

  2. nadine Says:

    please reply in my email address…
    thanks

  3. siatic nevrve Says:

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