Long-Term Recovery After Endothelial Colony-Forming Cells or Human Umbilical Cord Blood Cells Administration in a Rat Model of Neonatal Hypoxic-Ischemic Encephalopathy

Overview

Journal Stem Cells Transl Med

Publisher Oxford University Press

Specialties Cell Biology
Pharmacology

Date 2017 Oct 6

PMID 28980775

Citations 19

Authors

Isabelle Grandvuillemin

Philippe Garrigue

Alaa Ramdani

Farid Boubred

Umberto Simeoni

Francoise Dignat-George

Florence Sabatier

Benjamin Guillet

Affiliations

Soon will be listed here.

Abstract

Neonatal hypoxic-ischemic encephalopathy (NHIE) is a dramatic perinatal complication, associated with poor neurological prognosis despite neuroprotection by therapeutic hypothermia, in the absence of an available curative therapy. We evaluated and compared ready-to-use human umbilical cord blood cells (HUCBC) and bankable but allogeneic endothelial progenitors (ECFC) as cell therapy candidate for NHIE. We compared benefits of HUCBC and ECFC transplantation 48 hours after injury in male rat NHIE model, based on the Rice-Vannucci approach. Based on behavioral tests, immune-histological assessment and metabolic imaging of brain perfusion using single photon emission computed tomography (SPECT), HUCBC, or ECFC administration provided equally early and sustained functional benefits, up to 8 weeks after injury. These results were associated with total normalization of injured hemisphere cerebral blood flow assessed by SPECT/CT imaging. In conclusion, even if ECFC represent an efficient candidate, HUCBC autologous criteria and easier availability make them the ideal candidate for hypoxic-ischemic cell therapy. Stem Cells Translational Medicine 2017;6:1987-1996.

Citing Articles

Mononuclear cell therapy of neonatal hypoxic-ischemic encephalopathy in preclinical versus clinical studies: a systematic analysis of therapeutic efficacy and study design.

Scrutton A, Ollis F, Boltze J Neuroprotection. 2024; 1(2):143-159.

PMID: 38213793 PMC: 7615506. DOI: 10.1002/nep3.29.

Stem cell-based interventions for the treatment of stroke in newborn infants.

Bruschettini M, Badura A, Romantsik O Cochrane Database Syst Rev. 2023; 11:CD015582.

PMID: 37994736 PMC: 10666199. DOI: 10.1002/14651858.CD015582.pub2.

The alternative 3' splice site of may promote neuronal survival after neonatal hypoxic-ischemic encephalopathy injury.

Chen G, Yan S, Zhang J, Zhang J, Deng I, He R Ibrain. 2023; 8(3):302-313.

PMID: 37786733 PMC: 10529014. DOI: 10.1002/ibra.12056.

Umbilical Cord Blood-Derived Cell Therapy for Perinatal Brain Injury: A Systematic Review & Meta-Analysis of Preclinical Studies.

Nguyen T, Purcell E, Smith M, Penny T, Paton M, Zhou L Int J Mol Sci. 2023; 24(5).

PMID: 36901781 PMC: 10001969. DOI: 10.3390/ijms24054351.

Factors Influencing the Efficacy of Umbilical Cord Blood-Derived Cell Therapy for Perinatal Brain Injury.

Purcell E, Nguyen T, Smith M, Penny T, Paton M, Zhou L Stem Cells Transl Med. 2023; 12(3):125-139.

PMID: 36847059 PMC: 10021495. DOI: 10.1093/stcltm/szad006.

References

Fan L, Lin S, Pang Y, Lei M, Zhang F, Rhodes P . Hypoxia-ischemia induced neurological dysfunction and brain injury in the neonatal rat. Behav Brain Res. 2005; 165(1):80-90. DOI: 10.1016/j.bbr.2005.06.033. View

Azzopardi D, Strohm B, Edwards A, Dyet L, Halliday H, Juszczak E . Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med. 2009; 361(14):1349-58. DOI: 10.1056/NEJMoa0900854. View

Bae S, Kong T, Lee H, Kim K, Hong K, Chopp M . Long-lasting paracrine effects of human cord blood cells on damaged neocortex in an animal model of cerebral palsy. Cell Transplant. 2012; 21(11):2497-515. DOI: 10.3727/096368912X640457. View

Kaur C, Rathnasamy G, Ling E . Roles of activated microglia in hypoxia induced neuroinflammation in the developing brain and the retina. J Neuroimmune Pharmacol. 2012; 8(1):66-78. DOI: 10.1007/s11481-012-9347-2. View

Ingram D, Mead L, Tanaka H, Meade V, Fenoglio A, Mortell K . Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004; 104(9):2752-60. DOI: 10.1182/blood-2004-04-1396. View

Gluckman P, Wyatt J, Azzopardi D, Ballard R, Edwards A, Ferriero D . Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet. 2005; 365(9460):663-70. DOI: 10.1016/S0140-6736(05)17946-X. View

Aridas J, McDonald C, Paton M, Yawno T, Sutherland A, Nitsos I . Cord blood mononuclear cells prevent neuronal apoptosis in response to perinatal asphyxia in the newborn lamb. J Physiol. 2015; 594(5):1421-35. PMC: 4771799. DOI: 10.1113/JP271104. View

Li Y, Liang G, Wang S, Meng Q, Wang Q, Wei H . Effects of fetal exposure to isoflurane on postnatal memory and learning in rats. Neuropharmacology. 2007; 53(8):942-50. PMC: 2170454. DOI: 10.1016/j.neuropharm.2007.09.005. View

Ming-Yan H, Luo Y, Zhang X, Liu H, Gao R, Wu J . Hypoxic-ischemic injury decreases anxiety-like behavior in rats when associated with loss of tyrosine-hydroxylase immunoreactive neurons of the substantia nigra. Braz J Med Biol Res. 2011; 45(1):13-9. PMC: 3854134. DOI: 10.1590/s0100-879x2011007500161. View

10.

Cuccuini W, Poitevin S, Poitevin G, Dignat-George F, Cornillet-Lefebvre P, Sabatier F . Tissue factor up-regulation in proinflammatory conditions confers thrombin generation capacity to endothelial colony-forming cells without influencing non-coagulant properties in vitro. J Thromb Haemost. 2010; 8(9):2042-52. DOI: 10.1111/j.1538-7836.2010.03936.x. View

11.

Garrigue P, Hache G, Bennis Y, Brige P, Stalin J, Pellegrini L . Erythropoietin Pretreatment of Transplanted Endothelial Colony-Forming Cells Enhances Recovery in a Cerebral Ischemia Model by Increasing Their Homing Ability: A SPECT/CT Study. J Nucl Med. 2016; 57(11):1798-1804. DOI: 10.2967/jnumed.115.170308. View

12.

Renault-Mihara F, Okada S, Shibata S, Nakamura M, Toyama Y, Okano H . Spinal cord injury: emerging beneficial role of reactive astrocytes' migration. Int J Biochem Cell Biol. 2008; 40(9):1649-53. DOI: 10.1016/j.biocel.2008.03.009. View

13.

Lawn J, Cousens S, Zupan J . 4 million neonatal deaths: when? Where? Why?. Lancet. 2005; 365(9462):891-900. DOI: 10.1016/S0140-6736(05)71048-5. View

14.

Pimentel-Coelho P, Mendez-Otero R . Cell therapy for neonatal hypoxic-ischemic encephalopathy. Stem Cells Dev. 2009; 19(3):299-310. DOI: 10.1089/scd.2009.0403. View

15.

Levine S . Anoxic-ischemic encephalopathy in rats. Am J Pathol. 1960; 36:1-17. PMC: 1942188. View

16.

Bennis Y, Sarlon-Bartoli G, Guillet B, Lucas L, Pellegrini L, Velly L . Priming of late endothelial progenitor cells with erythropoietin before transplantation requires the CD131 receptor subunit and enhances their angiogenic potential. J Thromb Haemost. 2012; 10(9):1914-28. DOI: 10.1111/j.1538-7836.2012.04835.x. View

17.

Butovsky O, Talpalar A, Ben-Yaakov K, Schwartz M . Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol Cell Neurosci. 2005; 29(3):381-93. DOI: 10.1016/j.mcn.2005.03.005. View

18.

Shankaran S, Laptook A, Ehrenkranz R, Tyson J, McDonald S, Donovan E . Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med. 2005; 353(15):1574-84. DOI: 10.1056/NEJMcps050929. View

19.

Lehnardt S, Massillon L, Follett P, Jensen F, Ratan R, Rosenberg P . Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A. 2003; 100(14):8514-9. PMC: 166260. DOI: 10.1073/pnas.1432609100. View

20.

Codaccioni J, Velly L, Moubarik C, Bruder N, Pisano P, Guillet B . Sevoflurane preconditioning against focal cerebral ischemia: inhibition of apoptosis in the face of transient improvement of neurological outcome. Anesthesiology. 2009; 110(6):1271-8. DOI: 10.1097/ALN.0b013e3181a1fe68. View