Compression injury in the mouse spinal cord elicits a specific proliferative response and distinct cell fate acquisition along rostro-caudal and dorso-ventral axes

Neuroscience

Volumn 254, Issue , 2013, Pages 1-17

  McDonough, A ^a,b   Hoang, A N ^b   Monterrubio, A M ^a,b   Greenhalgh, S ^b   Martinez Cerdeno V ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

Author keywords

Cell fate; Precursor cells; Proliferation; Spinal cord injury

Indexed keywords

CELL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN; IBA1 PROTEIN; MAP2 PROTEIN; NESTIN; NEURON SPECIFIC NUCLEAR PROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN S100B; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG; AUTACOID;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; FEMALE; GLIA CELL; GRAY MATTER; MACROPHAGE; MICROGLIA; MITOSIS; MOUSE; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SPINAL CORD; SPINAL CORD COMPRESSION; SPINAL CORD NERVE CELL; SPINAL CORD REGENERATION; WHITE MATTER; ANIMAL; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPINAL CORD INJURY; VERTEBRA;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; INFLAMMATION MEDIATORS; MICE; SPINAL CORD COMPRESSION; SPINAL CORD INJURIES; THORACIC VERTEBRAE;

EID: 84885393428     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.09.011     Document Type: Article

References (52)

1. Barnabe-Heider F., Goritz C., Sabelstrom H., Takebayashi H., Pfrieger F.W., Meletis K., Frisen J. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 2010, 7:470-482.
2. Basso D.M., Beattie M.S., Bresnahan J.C. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 1996, 139:244-256.
3. Beattie M.S., Bresnahan J.C., Komon J., Tovar C.A., Van Meter M., Anderson D.K., Faden A.I., Hsu C.Y., Noble L.J., Salzman S., Young W. Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 1997, 148:453-463.
4. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63.
5. Chen C., Daugherty D., Jiang P., Deng W. Oligodendrocyte progenitor cells derived from mouse embryonic stem cells give rise to type-1 and type-2 astrocytes in vitro. Neurosci Lett 2012, 523:180-185.
6. Danilov A.I., Covacu R., Moe M.C., Langmoen I.A., Johansson C.B., Olsson T., Brundin L. Neurogenesis in the adult spinal cord in an experimental model of multiple sclerosis. Eur J Neurosci 2006, 23:394-400.
7. Eftekharpour E., Karimi-Abdolrezaee S., Fehlings M.G. Current status of experimental cell replacement approaches to spinal cord injury. Neurosurg Focus 2008, 24:E19.
8. Fouad K., Klusman I., Schwab M.E. Regenerating corticospinal fibers in the Marmoset (Callitrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. Eur J Neurosci 2004, 20:2479-2482.
9. Gensel J.C., Tovar C.A., Hamers F.P., Deibert R.J., Beattie M.S., Bresnahan J.C. Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J Neurotrauma 2006, 23:36-54.
10. Glass J.D., Boulis N.M., Johe K., Rutkove S.B., Federici T., Polak M., Kelly C., Feldman E.L. Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: results of a phase I trial in 12 patients. Stem Cells 2012, 30:1144-1151.
11. Grossman S.D., Rosenberg L.J., Wrathall J.R. Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp Neurol 2001, 168:273-282.
12. Hawryluk G.W., Rowland J., Kwon B.K., Fehlings M.G. Protection and repair of the injured spinal cord: a review of completed, ongoing, and planned clinical trials for acute spinal cord injury. Neurosurg Focus 2008, 25:E14.
13. Horky L.L., Galimi F., Gage F.H., Horner P.J. Fate of endogenous stem/progenitor cells following spinal cord injury. J Comp Neurol 2006, 498:525-538.
14. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J., Gage F.H. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 2000, 20:2218-2228.
15. Inman D., Guth L., Steward O. Genetic influences on secondary degeneration and wound healing following spinal cord injury in various strains of mice. J Comp Neurol 2002, 451:225-235.
16. Jakeman L.B., Guan Z., Wei P., Ponnappan R., Dzwonczyk R., Popovich P.G., Stokes B.T. Traumatic spinal cord injury produced by controlled contusion in mouse. J Neurotrauma 2000, 17:299-319.
17. Johansson C.B., Momma S., Clarke D.L., Risling M., Lendahl U., Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 1999, 96:25-34.
18. Karussis D., Karageorgiou C., Vaknin-Dembinsky A., Gowda-Kurkalli B., Gomori J.M., Kassis I., Bulte J.W., Petrou P., Ben-Hur T., Abramsky O., Slavin S. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010, 67:1187-1194.
19. Ke Y., Chi L., Xu R., Luo C., Gozal D., Liu R. Early response of endogenous adult neural progenitor cells to acute spinal cord injury in mice. Stem Cells 2006, 24:1011-1019.
20. Lee Y.S., Lin C.Y., Jiang H.H., Depaul M., Lin V.W., Silver J. Nerve regeneration restores supraspinal control of bladder function after complete spinal cord injury. J Neurosci 2013, 33:10591-10606.
21. Li Y., Zhang W.M., Wang T.H. Optimal location and time for neural stem cell transplantation into transected rat spinal cord. Cell Mol Neurobiol 2011, 31:407-414.
22. Liebscher T., Schnell L., Schnell D., Scholl J., Schneider R., Gullo M., Fouad K., Mir A., Rausch M., Kindler D., Hamers F.P., Schwab M.E. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann Neurol 2005, 58:706-719.
23. Lytle J.M., Wrathall J.R. Glial cell loss, proliferation and replacement in the contused murine spinal cord. Eur J Neurosci 2007, 25:1711-1724.
24. Marques S.A., Garcez V.F., Del Bel E.A., Martinez A.M. A simple, inexpensive and easily reproducible model of spinal cord injury in mice: morphological and functional assessment. J Neurosci Methods 2009, 177:183-193.
25. Mazzini L., Ferrero I., Luparello V., Rustichelli D., Gunetti M., Mareschi K., Testa L., Stecco A., Tarletti R., Miglioretti M., Fava E., Nasuelli N., Cisari C., Massara M., Vercelli R., Oggioni G.D., Carriero A., Cantello R., Monaco F., Fagioli F. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: a phase I clinical trial. Exp Neurol 2010, 223:229-237.
26. McDonough A., Martinez-Cerdeno V. Endogenous proliferation after spinal cord injury in animal models. Stem Cells Int 2012, 2012:387513.
27. McTigue D.M., Wei P., Stokes B.T. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci 2001, 21:3392-3400.
28. Meletis K., Barnabe-Heider F., Carlen M., Evergren E., Tomilin N., Shupliakov O., Frisen J. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 2008, 6:e182.
29. Menet V., Prieto M., Privat A., Gimenez y Ribotta M. Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proc Natl Acad Sci U S A 2003, 100:8999-9004.
30. Mothe A.J., Tator C.H. Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience 2005, 131:177-187.
31. Nakamura M., Houghtling R.A., MacArthur L., Bayer B.M., Bregman B.S. Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp Neurol 2003, 184:313-325.
32. Namiki J., Tator C.H. Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. J Neuropathol Exp Neurol 1999, 58:489-498.
33. Nishimura S., Yasuda A., Iwai H., Takano M., Kobayashi Y., Nori S., Tsuji O., Fujiyoshi K., Ebise H., Toyama Y., Okano H., Nakamura M. Time-dependent changes in the microenvironment of injured spinal cord affects the therapeutic potential of neural stem cell transplantation for spinal cord injury. Mol Brain 2013, 6:3.
34. Okano H., Sakaguchi M., Ohki K., Suzuki N., Sawamoto K. Regeneration of the central nervous system using endogenous repair mechanisms. J Neurochem 2007, 102:1459-1465.
35. Parr A.M., Kulbatski I., Tator C.H. Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J Neurotrauma 2007, 24:835-845.
36. Petit A., Sanders A.D., Kennedy T.E., Tetzlaff W., Glattfelder K.J., Dalley R.A., Puchalski R.B., Jones A.R., Roskams A.J. Adult spinal cord radial glia display a unique progenitor phenotype. PLoS ONE 2011, 6:e24538.
37. Piltti K.M., Salazar D.L., Uchida N., Cummings B.J., Anderson A.J. Safety of epicenter versus intact parenchyma as a transplantation site for human neural stem cells for spinal cord injury therapy. Stem Cells Transl Med 2013, 2:204-216.
38. Plemel J.R., Duncan G., Chen K.W., Shannon C., Park S., Sparling J.S., Tetzlaff W. A graded forceps crush spinal cord injury model in mice. J Neurotrauma 2008, 25:350-370.
39. Ruff R.L., McKerracher L., Selzer M.E. Repair and neurorehabilitation strategies for spinal cord injury. Ann N Y Acad Sci 2008, 1142:1-20.
40. Sellers D.L., Horner P.J. Instructive niches: environmental instructions that confound NG2 proteoglycan expression and the fate-restriction of CNS progenitors. J Anat 2005, 207:727-734.
41. Sellers D.L., Maris D.O., Horner P.J. Postinjury niches induce temporal shifts in progenitor fates to direct lesion repair after spinal cord injury. J Neurosci 2009, 29:6722-6733.
42. Stammers A.T., Liu J., Kwon B.K. Expression of inflammatory cytokines following acute spinal cord injury in a rodent model. J Neurosci Res 2012, 90:782-790.
43. Takahashi M., Arai Y., Kurosawa H., Sueyoshi N., Shirai S. Ependymal cell reactions in spinal cord segments after compression injury in adult rat. J Neuropathol Exp Neurol 2003, 62:185-194.
44. Tarasenko Y.I., Gao J., Nie L., Johnson K.M., Grady J.J., Hulsebosch C.E., McAdoo D.J., Wu P. Human fetal neural stem cells grafted into contusion-injured rat spinal cords improve behavior. J Neurosci Res 2007, 85:47-57.
45. Tu J., Liao J., Stoodley M.A., Cunningham A.M. Differentiation of endogenous progenitors in an animal model of post-traumatic syringomyelia. Spine 2010, 35:1116-1121. (Phila Pa 1976).
46. Vaquero J., Ramiro M.J., Oya S., Cabezudo J.M. Ependymal reaction after experimental spinal cord injury. Acta Neurochir (Wien) 1981, 55:295-302.
47. Vaquero J., Ramiro M.J., Oya S., Cabezudo J.M. Ependymal cell proliferation after spinal cord injury. Surg Neurol 1987, 28:401.
48. Watson C., Paxinos G., Kayalioglu G. The spinal cord: a Christopher and Dana Reeve foundation text and atlas 2009, Elsevier Science.
49. Weidner N., Ner A., Salimi N., Tuszynski M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci U S A 2001, 98:3513-3518.
50. Zai L.J., Wrathall J.R. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005, 50:247-257.
51. Zai L.J., Yoo S., Wrathall J.R. Increased growth factor expression and cell proliferation after contusive spinal cord injury. Brain Res 2005, 1052:147-155.
52. Zhang Z., Fujiki M., Guth L., Steward O. Genetic influences on cellular reactions to spinal cord injury: a wound-healing response present in normal mice is impaired in mice carrying a mutation (WldS) that causes delayed Wallerian degeneration. J Comp Neurol 1996, 371:485-495.