Reduction of Brain Injury in Neonatal Hypoxic—Ischemic Rats by Intracerebroventricular Injection of Neural Stem/Progenitor Cells Together With Chondroitinase ABC
Restricted accessResearch articleFirst published online July, 2008
Reduction of Brain Injury in Neonatal Hypoxic—Ischemic Rats by Intracerebroventricular Injection of Neural Stem/Progenitor Cells Together With Chondroitinase ABC
Perinatal hypoxia—ischemia (HI) remains a critical issue. Cell transplantation therapy could be a potent treatment for many neurodegenerative diseases, but limited works on this kind of therapy have been reported for perinatal HI. In this study, the therapeutic effect of transplantation with neural stem/ progenitor cells (NSPCs) and chondrotinase ABC (ChABC) in a neonatal HI rat model is evaluated. Histological studies showed that the unaffected area of the brain in animals treated with NSPCs together with ChABC was significantly larger than that in the animals treated with vehicle or NSPCs alone. The wet weight of the brain that received the combined treatment was also significantly higher than those of the vehicle and their individual treatments. These results indicate that intracerebroventricular injection of NSPCs with ChABC reduces brain injury in a rat neonatal HI model.
Lawn JE, Cousens S., Zupan J.4 million neonatal deaths: When? Where? Why?Lancet. 2005;365:891-900.
2.
Wagner CL, Eicher DJ, Katikaneni LD, Barbosa E., Holden KRThe use of hypothermia: a role in the treatment of neonatal asphyxia? Pediatr Neurol. 1999;21:429-443.
3.
Vannucci RC, Perlman JMInterventions for perinatal hypoxic-ischemic encephalopathy. Pediatrics. 1997;100:1004-1014.
4.
Levene MI, Evans DJ, Mason S., Brown J.An international network for evaluating neuroprotective therapy after severe birth asphyxia. Semin Perinatol. 1999;23:226-233.
5.
Gluckman PD,Wyatt JS, Azzopardi D., et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet . 2005; 365:663-670.
6.
Shankaran S. , Laptook AR, Ehrenkranz RA, et al.Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med. 2005;353:1574-1584.
7.
Shimazaki T.Biology and clinical application of neural stem cells. Horm Res. 2003;60(Suppl 3):1-9.
8.
Bithell A., Williams BPNeural stem cells and cell replacement therapy: making the right cells. Clin Sci (Lond). 2005;108:13-22.
9.
Conti L., Reitano E., Cattaneo E.Neural stem cell systems: diversities and properties after transplantation in animal models of diseases. Brain Pathol. 2006;16:143-154.
10.
Björklund A. , Lindvall O.Cell replacement therapies for central nervous system disorders. Nat Neurosci. 2000;3:537-544.
11.
Zheng T., Rossignol C., Leibovici A., Anderson KJ, Steindler DA,Weiss MDTransplantation of multipotent astrocytic stem cells into a rat model of neonatal hypoxic-ischemic encephalopathy. Brain Res. 2006;1112:99-105.
12.
Park KI, Hack MA, Ourednik J., et al. Acute injury directs the migration, proliferation, and differentiation of solid organ stem cells: evidence from the effect of hypoxia-ischemia in the CNS on clonal "reporter" neural stem cells. Exp Neurol . 2006;199:156-178.
13.
Park KI, Himes BT, Stieg PE, Tessler A., Fischer I., Snyder EYNeural stem cells may be uniquely suited for combined gene therapy and cell replacement: evidence from engraftment of Neurotrophin-3-expressing stem cells in hypoxic-ischemic brain injury. Exp Neurol. 2006;199:179-190.
14.
Ma J., Wang Y., Yang J., et al. Treatment of hypoxic-ischemic encephalopathy in mouse by transplantation of embryonic stem cell-derived cells. Neurochem Int. 2007;51:57-65.
15.
Yasuhara T. , Matsukawa N.,Yu G., et al. Transplantation of cryopreserved human bone marrow-derived multipotent adult progenitor cells for neonatal hypoxic-ischemic injury: targeting the hippocampus. Rev Neurosci. 2006;17:215-225.
16.
Oohira A., Matsui F., Tokita Y.,Yamauchi S., Aono S.Molecular interactions of neural chondroitin sulfate proteoglycans in the brain development. Arch Biochem Biophys. 2000 ;374:24-34.
17.
Silver J.Inhibitory molecules in development and regeneration. J Neurol . 1994;242:S22-S24.
18.
Bradbury EJ , Moon LD, Popat RJ, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 2002;416:636-640.
19.
Matsui F., Oohira A.Proteoglycans and injury of the central nervous system. Congenit Anom (Kyoto). 2004;44:181-188.
20.
Rhodes KE, Fawcett JWChondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J Anat. 2004;204:33-48.
21.
Ikegami T., Nakamura M.,Yamane J., et al. Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur J Neurosci. 2005;22:3036-3046.
22.
Sango K., Oohira A., Ajiki K., Tokashiki A., Horie M., Kawano H.Phosphacan and neurocan are repulsive substrata for adhesion and neurite extension of adult rat dorsal root ganglion neurons in vitro. Exp Neurol . 2003;182:1-11.
23.
Ida M., Shuo T., Hirano K., et al. Identification and functions of chondroitin sulfate in the milieu of neural stem cells. J Biol Chem. 2006;281:5982-5991.
24.
Rice JE III, Vannucci RC, Brierley JBThe influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol. 1981;9:131-141.
25.
Matsui F., Kakizawa H., Nishizuka M., et al. Changes in the amounts of chondroitin sulfate proteoglycans in rat brain after neonatal hypoxia-ischemia. J Neurosci Res . 2005;81:837-845.
26.
Kakizawa H., Matsui F., Tokita Y., et al. Neuroprotective effect of nipradilol, an NO donor, on hypoxic-ischemic brain injury of neonatal rats. Early Hum Dev. 2007;83:535-540.
27.
Jin K., Sun Y., Xie L., et al. Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat. Neurobiol Dis. 2005;18:366-374.
28.
Kelly S., Bliss TM, Shah AK, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A. 2004;101: 11839-11844.
29.
Llado J., Haenggeli C., Maragakis NJ, Snyder EY, Rothstein JDNeural stem cells protect against glutamate-induced excitotoxicity and promote survival of injured motor neurons through the secretion of neurotrophic factors . Mol Cell Neurosci. 2004; 27:322-331.
30.
Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett JW, Maffei L.Reactivation of ocular dominance plasticity in the adult visual cortex. Science. 2002;298:1248-1251.
31.
Corvetti L. , Rossi F.Degradation of chondroitin sulfate proteoglycans induces sprouting of intact Purkinje axons in the cerebellum of the adult rat. J Neurosci. 2005;25:7150-7158.
32.
Barritt AW, Davies M., Marchand F., et al. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci. 2006;26:10856-10867.
33.
Nandini CD, Sugahara K.Role of the sulfation pattern of chondroitin sulfate in its biological activities and in the binding of growth factors. Adv Pharmacol. 2006;53:253-279.
34.
Rolls A., Avidan H., Cahalon L., et al. A disaccharide derived from chondroitin sulphate proteoglycan promotes central nervous system repair in rats and mice. Eur J Neurosci. 2004;20: 1973-1983.
35.
Rolls A., Cahalon L., Bakalash S.,Avidan H., Lider O., Schwartz M.A sulfated disaccharide derived from chondroitin sulfate proteoglycan protects against inflammation-associated neurodegeneration. FASEB J . 2006;20:547-549.
36.
Ogawa Y., Sawamoto K., Miyata T., et al. Transplantation of in vitro-expanded fetal neural progenitor cells results in neuro-genesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res. 2002 ;69:925-933.
37.
Hagberg H., Gilland E., Bona E., et al. Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia-ischemia in neonatal rats. Pediatr Res. 1996;40:603-609.
38.
Nakajima W. , Ishida A., Lange MS, et al. Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci. 2000;20:7994-8004.
39.
Xia WJ,Yang M., Fok TF, et al. Partial neuroprotective effect of pretreatment with tanshinone IIA on neonatal hypoxia-ischemia brain damage. Pediatr Res . 2005;58:784-790.
40.
Vannucci RC , Connor JR, Mauger DT, et al. Rat model of perinatal hypoxic-ischemic brain damage. J Neurosci Res. 1999;55:158-163.
41.
Grow J., Barks JDPathogenesis of hypoxic-ischemic cerebral injury in the term infant: current concepts. Clin Perinatol. 2002;29:585-602, v.
42.
Northington FJBrief update on animal models of hypoxic-ischemic encephalopathy and neonatal stroke. ILAR J. 2006; 47:32-38.
43.
Sanberg PR, Willing AE, Garbuzova-Davis S., et al. Umbilical cord blood-derived stem cells and brain repair. Ann N Y Acad Sci. 2005;1049:67-83.
