Nestin-Positive Ependymal Cells Are Increased in the Human Spinal Cord after Traumatic Central Nervous System Injury

Journal of Neurotrauma

Volumn 32, Issue 18, 2015, Pages 1393-1402

  Cawsey, Thomas ^a   Duflou, Johan ^b   Weickert, Cynthia Shannon ^c,d,e   Gorrie, Catherine Anne ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b NSW Health Pathology Western   (Australia)

^c NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^d Sydney Genetics   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

GFAP; neural progenitor cells; postmortem; tanyctye; trauma

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; NES PROTEIN, HUMAN;

ADOLESCENT; ADULT; ARTICLE; AUTOPSY; CENTRAL NERVOUS SYSTEM DISEASE; CENTRAL NERVOUS SYSTEM INJURY; CERVICAL SPINAL CORD; CHILD; CLINICAL ARTICLE; EPENDYMA CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; LUMBAR SPINAL CORD; MALE; NEURAL STEM CELL; SURVIVAL TIME; THORACIC SPINAL CORD; BRAIN INJURY; CELL SURVIVAL; EPENDYMA; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INFANT; METABOLISM; NEWBORN; PATHOLOGY; PREGNANCY; PRESCHOOL CHILD; SPINAL CORD; YOUNG ADULT;

ADOLESCENT; ADULT; BRAIN INJURIES; CELL SURVIVAL; CHILD; CHILD, PRESCHOOL; EPENDYMA; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INFANT; INFANT, NEWBORN; NESTIN; NEURAL STEM CELLS; PREGNANCY; SPINAL CORD; YOUNG ADULT;

EID: 84941214778     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2014.3575     Document Type: Article

References (38)

1. Eriksson, P.S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A., and Gage, F.H. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317.
2. Taupin, P., and Gage, F.H. (2002). Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69, 745-749.
3. Kehl, L.J., Fairbanks, C.A., Laughlin, T.M., and Wilcox, G.L. (1997). Neurogenesis in postnatal rat spinal cord: a study in primary culture. Science 276, 586-589.
4. Cizkova, D., Nagyova, M., Slovinska, L., Novotna, I., Radonak, J., Cizek, M., Mechirova, E., Tomori, Z., Hlucilova, J., Motlik, J., Sulla, I., Jr., and Vanicky, I. (2009). Response of ependymal progenitors to spinal cord injury or enhanced physical activity in adult rat. Cell. Mol. Neurobiol. 29, 999-1013.
5. Meletis, K., Barnabe-Heider, F., Carlen, M., Evergren, E., Tomilin, N., Shupliakov, O., and Frisen, J. (2008). Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6, e182.
6. Weiss, S., Dunne, C., Hewson, J., Wohl, C., Wheatley, M., Peterson, A.C., and Reynolds, B.A. (1996). Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16, 7599-609.
7. Moreno-Manzano, V., Rodriguez-Jimenez, F.J., Garcia-Rosello, M., Lainez, S., Erceg, S., Calvo, M.T., Ronaghi, M., Lloret, M., Planells-Cases, R., Sanchez-Puelles, J.M., and Stojkovic, M. (2009). Activated spinal cord ependymal stem cells rescue neurological function. Stem Cells 27, 733-743.
8. Hamilton, L.K., Truong, M.K., Bednarczyk, M.R., Aumont, A., and Fernandes, K.J. (2009). Cellular organization of the central canal ependymal zone, a niche of latent neural stem cells in the adult mammalian spinal cord. Neuroscience 164, 1044-1056.
9. Tzeng, S.F. (2002). Neural progenitors isolated from newborn rat spinal cords differentiate into neurons and astroglia. J. Biomed. Sci. 9, 10-16.
10. Kojima, A., and Tator, C.H. (2000). Epidermal growth factor and fibroblast growth factor 2 cause proliferation of ependymal precursor cells in the adult rat spinal cord in vivo. J.Neuropathol.Exp.Neurol. 59, 687-697.
11. Mothe, A.J., and Tator, C.H. (2005). Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience 131, 177-187.
12. Blasko, J., Martoncikova, M., Lievajova, K., Saganova, A., and Racekova, E. (2012). Regional differences of proliferation activity in the spinal cord ependyma of adult rats. Cent. Eur. J. Biology 7, 397-403.
13. Horner, P.J., Power, A.E., Kempermann, G., Kuhn, H.G., Palmer, T.D., Winkler, J., Thal, L.J., and Gage, F.H. (2000). Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 20, 2218-2228.
14. Barnabe-Heider, F., Goritz, C., Sabelstrom, H., Takebayashi, H., Pfrieger, F.W., Meletis, K., and Frisen, J. (2010). Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7, 470-482.
15. Zai, L.J., and Wrathall, J.R. (2005). Cell proliferation and replacement following contusive spinal cord injury. Glia 50, 247-257.
16. Johansson, C.B., Momma, S., Clarke, D.L., Risling, M., Lendahl, U., and Frisen, J. (1999). Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96, 25-34.
17. Dromard, C., Guillon, H., Rigau, V., Ripoll, C., Sabourin, J.C., Perrin, F.E., Scamps, F., Bozza, S., Sabatier, P., Lonjon, N., Duffau, H., Vachiery-Lahaye, F., Prieto,M., TranVanBa, C.,Deleyrolle, L., Boularan,A., Langley,K.,Gaviria,M., Privat,A.,Hugnot, J.P., and Bauchet, L. (2008). Adult human spinal cord harbors neural precursor cells that generate neurons and glial cells in vitro. J. Neurosci. Res. 86, 1916-1926.
18. Mothe, A.J., Zahir, T., Santaguida, C., Cook, D., and Tator, C.H. (2011). Neural stem/progenitor cells from the adult human spinal cord are multipotent and self-renewing and differentiate after transplantation. PLoS One 6, e27079.
19. Snethen, H., Love, S., and Scolding, N. (2008). Disease-responsive neural precursor cells are present in multiple sclerosis lesions. Regen. Med. 3, 835-847.
20. Sakakibara, A., Aoki, E., Hashizume, Y., Mori, N., and Nakayama, A. (2007). Distribution of nestin and other stem cell-related molecules in developing and diseased human spinal cord. Pathol. Int. 57, 358-368.
21. Takano, T., and Becker, L.E. (1997). Overexpression of nestin and vimentin in the ependyma of spinal cords from hydrocephalic infants. Neuropathol. Appl. Neurobiol. 23, 3-15.
22. Alfaro-Cervello, C., Soriano-Navarro, M., Mirzadeh, Z., Alvarez-Buylla, A., and Garcia-Verdugo, J.M. (2011). Biciliated ependymal cell proliferation contributes to spinal cord growth. J. Comp. Neurol. 520, 3528-3552.
23. Bruni, J.E., and Reddy, K. (1987). Ependyma of the central canal of the rat spinal cord: a light and transmission electron microscopic study. J. Anat. 152, 55-70.
24. Bruni, J.E., Del Bigio, M.R., and Clattenburg, R.E. (1985). Ependyma: normal and pathological.Areviewof the literature. Brain Res. 356, 1-19.
25. Bruni, J.E. (1998). Ependymal development, proliferation, and functions: a review. Microsc Res Tech 41, 2-13.
26. Rodr?guez, E.M., Blazquez, J.L., Pastor, F.E., Pelaez, B., Pena, P., Peruzzo, B., and Amat, P. (2005). Hypothalamic tanycytes: a key component of brain-endocrine interaction. international review of cytology. 247, 89-167.
27. Xu, Y., Tamamaki, N., Noda, T., Kimura, K., Itokazu, Y., Matsumoto, N., Dezawa, M., and Ide, C. (2005). Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp. Neurol. 192, 251-264.
28. Rafols, J.A., and Goshgarian, H.G. (1985). Spinal tanycytes in the adult rat: a correlative Golgi gold-toning study. Anat. Rec. 211, 75-86.
29. Namiki, J., and Tator, C.H. (1999). Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. J. Neuropathol. Exp. Neurol. 58, 489-498.
30. Xu, R., Wu, C., Tao, Y., Yi, J., Yang, Y., Zhang, X., and Liu, R. (2008). Nestin-positive cells in the spinal cord: a potential source of neural stem cells. Int. J. Dev. Neurosci. 26, 813-820.
31. Lendahl, U., Zimmerman, L.B., and McKay, R.D. (1990). CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595.
32. Li, Y., and Chopp, M. (1999). Temporal profile of nestin expression after focal cerebral ischemia in adult rat. Brain Res. 838, 1-10.
33. Nakayama, D., Matsuyama, T., Ishibashi-Ueda, H., Nakagomi, T., Kasahara, Y., Hirose, H., Kikuchi-Taura, A., Stern, D.M., Mori, H., and Taguchi, A. (2010). Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex. Eur. J. Neurosci. 31, 90-98.
34. Gorrie, C., Oakes, S., Duflou, J., Blumbergs, P., and Waite, P.M. (2002). Axonal injury in children after motor vehicle crashes: extent, distribution, and size of axonal swellings using beta-APP immunohistochemistry. J. Neurotrauma 19, 1171-1182.
35. Hortobagyi, T., Wise, S., Hunt, N., Cary, N., Djurovic, V., Fegan-Earl, A., Shorrock, K., Rouse, D., and Al-Sarraj, S. (2007). Traumatic axonal damage in the brain can be detected using beta-APP immunohistochemistry within 35 min after head injury to human adults. Neuropathol. Appl. Neurobiol. 33, 226-237.
36. Frisen, J., Johansson, C.B., Torok, C., Risling, M., and Lendahl, U. (1995). Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J. Cell Biol. 131, 453-464.
37. Takahashi, M., Arai, Y., Kurosawa, H., Sueyoshi, N., and Shirai, S. (2003). Ependymal cell reactions in spinal cord segments after compression injury in adult rat. J. Neuropathol. Exp. Neurol. 62, 185-194.
38. Jordan, F.L., Rieke, G.K., and Thomas, W.E. (1987). Presence and development of ependymal cells in primary tissue cultures derived from embryonic rat cerebral cortex. Brain Res. 432, 97-110.