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Arrested development of the dorsal column following neonatal spinal cord injury in the opossum, Monodelphis domestica

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Abstract

Developmental studies of spinal cord injury in which regrowth of axons occurs across the site of transection rarely distinguish between the recovery of motor-controlling pathways and that of ascending axons carrying sensory information. We describe the morphological changes that occur in the dorsal column (DC) of the grey short-tailed opossum, Monodelphis domestica, following spinal cord injury at two early developmental ages. The spinal cords of opossums that had had their mid-thoracic spinal cords completely transected at postnatal day 7 (P7) or P28 were analysed. Profiles of neurofilament immunoreactivity in transected cords showing DC development were differentially affected by the injury compared with the rest of the cord and cytoarchitecture was modified in an age- and site-dependent manner. The ability of DC neurites to grow across the site of transection was confirmed by injection of fluorescent tracer below the injury. P7 transected cords showed labelling in the DC above the site of original transection indicating that neurites of this sensory tract were able to span the injury. No growth of any neuronal processes was seen after P28 transection. Thus, DC is affected by spinal injury in a differential manner depending on the age at which the transection occurs. This age-differential response, together with other facets of remodelling that occur after neonatal spinal injury, might explain the locomotor adaptations and recovery observed in these animals.

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References

  • Cassidy G, Boudrias D, Pflieger JF, Cabana T (1994) The development of sensorimotor reflexes in the Brazilian opossum Monodelphis domestica. Brain Behav Evol 43:244–253

    Article  CAS  PubMed  Google Scholar 

  • Courtine G, Song B, Roy RR, Zhong H, Herrmann JE, Ao Y, Qi J, Edgerton VR, Sofroniew MV (2008) Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med 14:69–74

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Courtine G, Gerasimenko Y, Brand R van den, Yew A, Musienko P, Zhong H, Song B, Ao Y, Ichiyama RM, Lavrov I, Roy RR, Sofroniew MV, Edgerton VR (2009) Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 12:1333–1342

  • Cummings JP, Bernstein DR, Stelzner DJ (1981) Further evidence that sparing of function after spinal cord transection in the neonatal rat is not due to axonal generation or regeneration. Exp Neurol 74:615–620

    Article  CAS  PubMed  Google Scholar 

  • Dziegielewska KM, Habgood M, Jones SE, Reader M, Saunders NR (1989) Proteins in cerebrospinal fluid and plasma of postnatal Monodelphis domestica (grey short-tailed opossum). Comp Biochem Physiol B 92:569–576

    CAS  PubMed  Google Scholar 

  • Fadem BH, Trupin GL, Maliniak E, VandeBerg JL, Hayssen V (1982) Care and breeding of the gray, short-tailed opossum (Monodelphis domestica). Lab Anim Sci 32:405–409

    CAS  PubMed  Google Scholar 

  • Fry EJ, Saunders NR (2000) Spinal repair in immature animals: a novel approach using the South American opossum Monodelphis domestica. Clin Exp Pharmacol Physiol 27:542–547

    Article  CAS  PubMed  Google Scholar 

  • Fry EJ, Stolp HB, Lane MA, Dziegielewska KM, Saunders NR (2003) Regeneration of supraspinal axons after complete transection of the thoracic spinal cord in neonatal opossums (Monodelphis domestica). J Comp Neurol 466:422–444

    Article  PubMed  Google Scholar 

  • Gerasimenko YP, Ichiyama RM, Lavrov IA, Courtine G, Cai L, Zhong H, Roy RR, Edgerton VR (2007) Epidural spinal cord stimulation plus quipazine administration enable stepping in complete spinal adult rats. J Neurophysiol 98:2525–2536

    Article  CAS  PubMed  Google Scholar 

  • Gingras J, Cabana T (1999) Synaptogenesis in the brachial and lumbosacral enlargements of the spinal cord in the postnatal opossum, Monodelphis domestica. J Comp Neurol 414:551–560

    Article  CAS  PubMed  Google Scholar 

  • Lane MA, Truettner JS, Brunschwig JP, Gomez A, Bunge MB, Dietrich WD, Dziegielewska KM, Ek CJ, Vandeberg JL, Saunders NR (2007) Age-related differences in the local cellular and molecular responses to injury in developing spinal cord of the opossum, Monodelphis domestica. Eur J Neurosci 25:1725–1742

    Article  CAS  PubMed  Google Scholar 

  • Lavrov I, Courtine G, Dy CJ, Brand R van den, Fong AJ, Gerasimenko Y, Zhong H, Roy RR, Edgerton VR (2008a) Facilitation of stepping with epidural stimulation in spinal rats: role of sensory input. J Neurosci 28:7774–7780

  • Lavrov I, Dy CJ, Fong AJ, Gerasimenko Y, Courtine G, Zhong H, Roy RR, Edgerton VR (2008b) Epidural stimulation induced modulation of spinal locomotor networks in adult spinal rats. J Neurosci 28:6022–6029

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liddelow SA, Dziegielewska KM, Ek CJ, Johansson PA, Potter AM, Saunders NR (2009) Cellular transfer of macromolecules across the developing choroid plexus of Monodelphis domestica. Eur J Neurosci 29:253–266

    Article  PubMed  Google Scholar 

  • Martin GF, Beattie MS, Bresnahan JC, Henkel CK, Hughes HC (1975) Cortical and brain stem projections to the spinal cord of the American opossum, Didelphis marsupialis virginiana. Brain Behav Evol 12:270–310

    Article  CAS  PubMed  Google Scholar 

  • Migliavacca A (1928) La rigenerazione del midollo spinale nei feti e nei neonati. Boll Soc Med Chir Pavia 6:1147–1151

    Google Scholar 

  • Noor NM, Steer DL, Wheaton BJ, Ek CJ, Truettner JS, Dietrich WD, Dziegielewska KM, Richardson SJ, Smith AI, VandeBerg JL, Saunders NR (2011) Age-dependent changes in the proteome following complete spinal cord transection in a postnatal South American opossum (Monodelphis domestica). PLoS One 6:e27465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noor NM, Mollgard K, Wheaton BJ, Steer DL, Truettner JS, Dziegielewska KM, Dietrich WD, Smith AI, Saunders NR (2013) Expression and cellular distribution of ubiquitin in response to injury in the developing spinal cord of Monodelphis domestica. PLoS One 8:e62120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Petruska JC, Ichiyama RM, Jindrich DL, Crown ED, Tansey KE, Roy RR, Edgerton VR, Mendell LM (2007) Changes in motoneuron properties and synaptic inputs related to step training after spinal cord transection in rats. J Neurosci 27:4460–4471

    Article  CAS  PubMed  Google Scholar 

  • Pflieger JF, Cassidy G, Cabana T (1996) Development of spontaneous locomotor behaviors in the opossum, Monodelphis domestica. Behav Brain Res 80:137–143

    Article  CAS  PubMed  Google Scholar 

  • Qin YQ, Wang XM, Martin GF (1993) The early development of major projections from caudal levels of the spinal cord to the brainstem and cerebellum in the gray short-tailed Brazilian opossum, Monodelphis domestica. Brain Res Dev Brain Res 75:75–90

    Article  CAS  PubMed  Google Scholar 

  • Saunders NR, Dziegielewska KM (2000) Recovery from injury in the immature mammalian spinal cord. In: Saunders NR, Dziegielewska KM (eds) Degeneration and regeneration in the nervous system. Harwood Academic, Amsterdam, pp 17–52

    Google Scholar 

  • Saunders NR, Adam E, Reader M, Mollgard K (1989) Monodelphis domestica (grey short-tailed opossum): an accessible model for studies of early neocortical development. Anat Embryol (Berl) 180:227–236

    Article  CAS  Google Scholar 

  • Saunders NR, Balkwill P, Knott G, Habgood MD, Mollgard K, Treherne JM, Nicholls JG (1992) Growth of axons through a lesion in the intact CNS of fetal rat maintained in long-term culture. Proc Biol Sci 250:171–180

    Article  CAS  PubMed  Google Scholar 

  • Saunders NR, Deal A, Knott GW, Varga ZM, Nicholls JG (1995) Repair and recovery following spinal cord injury in a neonatal marsupial (Monodelphis domestica). Clin Exp Pharmacol Physiol 22:518–526

    Article  CAS  PubMed  Google Scholar 

  • Saunders NR, Kitchener P, Knott GW, Nicholls JG, Potter A, Smith TJ (1998) Development of walking, swimming and neuronal connections after complete spinal cord transection in the neonatal opossum, Monodelphis domestica. J Neurosci 18:339–355

    CAS  PubMed  Google Scholar 

  • Schnell L, Schwab ME (1993) Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur J Neurosci 5:1156–1171

    Article  CAS  PubMed  Google Scholar 

  • Schwab ME, Bartholdi D (1996) Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76:319–370

    CAS  PubMed  Google Scholar 

  • Terman JR, Wang XM, Martin GF (1999) Developmental plasticity of ascending spinal axons studies using the North American opossum, Didelphis virginiana. Brain Res Dev Brain Res 112:65–77

    Article  CAS  PubMed  Google Scholar 

  • Terman JR, Wang XM, Martin GF (2000) Repair of the transected spinal cord at different stages of development in the North American opossum, Didelphis virginiana. Brain Res Bull 53:845–855

    Article  CAS  PubMed  Google Scholar 

  • Tillakaratne NJ, Guu JJ, Leon RD de, Bigbee AJ, London NJ, Zhong H, Ziegler MD, Joynes RL, Roy RR, Edgerton VR (2010) Functional recovery of stepping in rats after a complete neonatal spinal cord transection is not due to regrowth across the lesion site. Neuroscience 166:23–33

  • Wang XM, Terman JR, Martin GF (1996) Evidence for growth of supraspinal axons through the lesion after transection of the thoracic spinal cord in the developing opossum Didelphis virginiana. J Comp Neurol 371:104–115

    Article  CAS  PubMed  Google Scholar 

  • Wang XM, Basso DM, Terman JR, Bresnahan JC, Martin GF (1998a) Adult opossums (Didelphis virginiana) demonstrate near normal locomotion after spinal cord transection as neonates. Exp Neurol 151:50–69

    Article  CAS  PubMed  Google Scholar 

  • Wang XM, Terman JR, Martin GF (1998b) Regeneration of supraspinal axons after transection of the thoracic spinal cord in the developing opossum, Didelphis virginiana. J Comp Neurol 398:83–97

    Article  CAS  PubMed  Google Scholar 

  • Whalley K, O’Neill P, Ferretti P (2006) Changes in response to spinal cord injury with development: vascularization, hemorrhage and apoptosis. Neuroscience 137:821–832

    Article  CAS  PubMed  Google Scholar 

  • Wheaton BJ, Callaway JK, Ek CJ, Dziegielewska KM, Saunders NR (2011) Spontaneous development of full weight-supported stepping after complete spinal cord transection in the neonatal opossum, Monodelphis domestica. PLoS One 6:e26826

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wheaton BJ, Noor NM, Whish SC, Truettner JS, Dietrich WD, Zhang M, Crack PJ, Dziegielewska KM, Saunders NR (2013) Weight-bearing locomotion in the developing opossum, Monodelphis domestica following spinal transection: remodeling of neuronal circuits caudal to lesion. PLoS One 8:e71181

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology and Therapeutics, The University of Melbourne, Parkville, VIC, Australia

    Benjamin J. Wheaton, Natassya M. Noor, Katarzyna M. Dziegielewska, Sophie Whish & Norman R. Saunders

  2. Department of Biology, University of New Mexico, Albuquerque, N.M., USA

    Benjamin J. Wheaton

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  1. Benjamin J. Wheaton
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  2. Natassya M. Noor
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  3. Katarzyna M. Dziegielewska
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  4. Sophie Whish
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  5. Norman R. Saunders
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Correspondence to Benjamin J. Wheaton.

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Wheaton, B.J., Noor, N.M., Dziegielewska, K.M. et al. Arrested development of the dorsal column following neonatal spinal cord injury in the opossum, Monodelphis domestica . Cell Tissue Res 359, 699–713 (2015). https://doi.org/10.1007/s00441-014-2067-6

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  • DOI: https://doi.org/10.1007/s00441-014-2067-6

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