[en] Neurological disorders are among the main clinical problems affecting preterm children and often result in the development of communication and learning disabilities later in life. Several factors are of importance for brain development, however the role of immunoglobulins (passive immunity transfer) has not yet been investigated. Piglets are born agammaglobulinemic, as a result of the lack of transfer of maternal immunoglobulins in utero, thus, they serve as an ideal model to mimic the condition of immunoglobulin deficiency in preterm infants. Thirty six, unsuckled newborn piglets were fed an infant formula or colostrum and supplemented orally or intravenously with either species-specific or foreign immunoglobulin and then compared to both newborn and sow-reared piglets. Two days after the piglets were born behavioural tests (novel recognition and olfactory discrimination of conspecifics scent) were performed, after which the piglets were sacrificed and blood, cerebrospinal fluid and hippocampi samples were collected for analyses. Both parameters of neuronal plasticity (neuronal maturation and synapse-associated proteins) and behavioural test parameters appeared to be improved by the appearance of species-specific porcine immunoglulin in the circulation and cerebrospinal fluid of the piglets. In conclusion, we postulate possible positive clinical effects following intravenous infusion of human immunoglobulin in terms of neuronal plasticity and cognitive function in preterm infants born with low blood immunoglobulin levels.
Disciplines :
Pediatrics
Author, co-author :
Goncharova, Kateryna
Lozinska, Liudmyla
Arevalo Sureda, Ester ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions animales et nutrition
Wolinski, Jaroslaw
Westrom, Bjorn
Pierzynowski, Stefan
Language :
English
Title :
Importance of neonatal immunoglobulin transfer for hippocampal development and behaviour in the newborn pig.
Publication date :
2017
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, United States - California
Foulder-Hughes LA, Cooke RW. Motor, cognitive, and behavioural disorders in children born very preterm. Dev Med Child Neurol. 2003; 45(2): 97-103. PMID: 12578235
Sutton PS, Darmstadt GL. Preterm birth and neurodevelopment: a review of outcomes and recommendations for early identification and cost-effective interventions. J Trop Pediatr.2013; 59(4): 258-265. https://doi.org/10.1093/tropej/fmt012 PMID: 23486391
Salmaso N, Jablonska B, Scafidi J, Vaccarino FM, Gallo V. Neurobiology of premature brain injury. Nat Neurosci. 2014; 17(3): 341-346. https://doi.org/10.1038/nn.3604 PMID: 24569830
Fischi-Gómez E, Vasung L, Meskaldji DE, Lazeyras F, Borradori-Tolsa C, Hagmann P, et al. Structural brain connectivity in school-age preterm infants provides evidence for impaired networks relevant for higher order cognitive skills and social cognition. Cereb Cortex. 2015; 25(9): 2793-2805. https://doi.org/10.1093/cercor/bhu073 PMID: 24794920
Pavlova MA, Krägeloh-Mann I. Limitations on the developing preterm brain: impact of periventricular white matter lesions on brain connectivity and cognition. Brain.2013; 136(Pt 4): 998-1011. https://doi.org/10.1093/brain/aws334 PMID: 23550112
Pandit AS, Robinson E, Aljabar P, Ball G, Gousias IS, Wang Z, et al. Whole-brain mapping of structural connectivity in infants reveals altered connection strength associated with growth and preterm birth. Cereb Cortex. 2014; 24(9): 2324-2333. https://doi.org/10.1093/cercor/bht086 PMID: 23547135
Nosarti C, Nam KW, Walshe M, Murray RM, Cuddy M, Rifkin L, Allin MP. Preterm birth and structural brain alterations in early adulthood. Neuroimage Clin. 2014; 6: 180-191. https://doi.org/10.1016/j.nicl.2014.08.005 PMID: 25379430
Palmeira P, Quinello C, Silveira-Lessa AL, Zago CA, Carneiro-Sampaio M. IgG placental transfer in healthy and pathological pregnancies. Clin Dev Immunol. 2012; 985646. https://doi.org/10.1155/2012/985646 PMID: 22235228
van den Berg JP, Westerbeek EA, van der Klis FR, Berbers GA, van Elburg RM. Transplacental transport of IgG antibodies to preterm infants: a review of the literature. Early Hum Dev. 2011; 87(2):67-72. https://doi.org/10.1016/j.earlhumdev.2010.11.003 PMID: 21123010
Alkan Ozdemir S, Ozer EA, Kose S, Ilhan O, Ozturk C, Sutcuoglu S. Reference values of serum IgG and IgM levels in preterm and term newborns. J Matern Fetal Neonatal Med. 2016; 29(6): 972-976. https://doi.org/10.3109/14767058.2015.1027680 PMID: 25845271
Bayry J, Misra N, Latry V, Prost F, Delignat S, Lacroix-Desmazes S, Kazatchkine MD, Kaveri SV. Mechanisms of action ofintravenous immunoglobulin in autoimmune and inflammatory diseases. Transfus Clin Biol. 2003; 10(3): 165-169. PMID: 12798851
Di Rosa R, Pietrosanti M, Luzi G, Salemi S, D'Amelio R. Polyclonal intravenous immunoglobulin: an important additional strategy in sepsis? Eur J Intern Med. 2014; 25(6): 511-516. https://doi.org/10.1016/j.ejim.2014.05.002 PMID: 24877856
Oygucu SE, Ozbudak IH, Akcan AB, Coskun M, Ozel D, Ozbilim G, Oygur N. Effects of high-dose intravenous immunoglobulin on lipopolysaccharide-induced acute lung injury. Int Immunopharmacol. 2014; 21(1): 51-55. https://doi.org/10.1016/j.intimp.2014.04.002 PMID: 24747095
Relkin N. Intravenous immunoglobulin for Alzheimer's disease. Clin Exp Immunol. 2014; 178 (Suppl 1): 27-29.
Lünemann JD, Quast I, Dalakas MC. Efficacy of Intravenous Immunoglobulin in Neurological Diseases. Neurotherapeutics. 2016; 13(1): 34-46. https://doi.org/10.1007/s13311-015-0391-5 PMID: 26400261
Pierzynowski S, Ushakova G, Kovalenko T, Osadchenko I, Goncharova K, Gustavsson P, et al. Impact of colostrum and plasma immunoglobulin intake on hippocampus structure during early postnatal development in pigs. Int J Dev Neurosci. 2014; 35: 64-71. https://doi.org/10.1016/j.ijdevneu.2014.03.003 PMID: 24642047
Socha-Banasiak A, Pierzynowski S, Woliński J, Grujic D, Boryczka M, Grzesiak P, et al. The pig as a model for premature infants-the importance ofimmunoglobulin supplementation for growth and development. J Biol Regul Homeost Agents. 2017; 31(1): 87-92. PMID: 28337875
Eiby YA, Wright LL, Kalanjati VP, Miller SM, Bjorkman ST, Keates HL, Lumbers ER, et al. A pig model of the preterm neonate: anthropometric and physiological characteristics. PLoS One.2013; 8(7): e68763. https://doi.org/10.1371/journal.pone.0068763 PMID: 23874755
Nguyen DN, Jiang P, Frøkiñr H, Heegaard PM, Thymann T, Sangild PT. Delayed development of systemic immunity in preterm pigs as a model for preterm infants. Sci Rep. 2016; 6: 36816. https://doi.org/10.1038/srep36816 PMID: 27830761
Grodzki AC, Berenstein E. Antibody purification: ammonium sulfate fractionation or gel filtration. Methods in Molecular Biology. 2010; 588: 15-26. https://doi.org/10.1007/978-1-59745-324-0-3 PMID: 20012814
Andersen AD, Sangild PT, Munch SL, van der Beek EM, Renes IB, Ginneken Cv, et al. Delayed growth, motor function and learning in preterm pigs during early postnatal life. Am J Physiol Regul Integr Comp Physiol. 2016; 310(6): R481-492. https://doi.org/10.1152/ajpregu.00349.2015 PMID: 26764054
Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process. 2012; 13: 93-110.https://doi.org/10.1007/s10339-011-0430-z PMID: 22160349
Andersen AD, Sangild PT, Munch SL, van der Beek EM, Renes IB, Ginneken Cv, et al. Delayed growth, motor function and learning in preterm pigs during early postnatal life. Am J Physiol Regul Integr Comp Physiol. 2016; 310(6): R481-492. https://doi.org/10.1152/ajpregu.00349.2015 PMID: 26764054
Kornum BR, Thygesen KS, Nielsen TR, Knudsen GM, Lind NM. The effect of the inter-phase delay interval in the spontaneous object recognition test for pigs. Behav Brain Res.2007; 181: 210-217. https://doi.org/10.1016/j.bbr.2007.04.007 PMID: 17524499
Ennaceur A, Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1. Behavioral data. Behav Brain Res. 1988; 31: 47-59. PMID: 3228475
Botton PH, Costa MS, Ardais AP, Mioranzza S, Souza DO, da Rocha JB, et al. Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav Brain Res. 2010; 214: 254-259. https://doi.org/10.1016/j.bbr.2010.05. 034 PMID: 20553765
Kristensen HH, Jones RB, Schofield CP, White RP, Wathes CM. The use of olfactory and other cues for social recognition by juvenile pigs. Appl Anim Behav Sci. 2001; 72(4): 321-333. PMID: 11348681
Modanlou HD, Beharry K, Bottoli I, Raghavender B, Aranda JV. Changes in cerebrospinal fluid and cerebrovascular endothelin concentrations during hypotension and hypertension in newborn piglets with induced sterile meningitis. Can J Physiol Pharmacol. 1996; 74(4): 368-375. PMID: 8828883
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. Journal Biol Chem. 1951; 193(1): 265-275.
Fahey JL, McKelvey EM. Quantitative determination of serum immunoglobulins in antibody-agar plates. J Immunol. 1965; 94: 84-90. PMID: 14253527
Zinchuk V, Zinchuk O, Okada T. Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem.2007; 40(4): 101-111. https://doi.org/10.1267/ahc.07002 PMID: 17898874
Shen RL, Thymann T, Østergaard MV, Støy AC, Krych è, Nielsen DS, et al. Early gradual feeding with bovine colostrum improves gut function and NEC resistance relative to infant formula in preterm pigs. Am J Physiol Gastrointest Liver Physiol. 2015; 309(5): G310-323. https://doi.org/10.1152/ajpgi.00163. 2015 PMID: 26138468
https://clinicaltrials.gov/ct2/show/NCT02054091, accessed February 2017.
Harada E, Araki Y, Furumura E, Takeuchi T, Sitizyo K, Yajima T, et al: Characteristic transfer of colostrum-derived biologically active substances into cerebrospinal fluid via blood in natural suckling neonatal pigs. J Vet Med A Physiol Pathol Clin Med.2002; 49(7): 358-364. PMID: 12440791
Erzurumlu RS, Jhaveri S, Benowitz LI. Transient patterns of GAP-43 expression during the formation of barrels in the rat somatosensory cortex. J Comp Neurol. 1990; 292: 443-456. https://doi.org/10.1002/cne.902920310 PMID: 2160480
Sretavan DW, Kruger K. Randomized retinal ganglion cell axon routing at the optic chiasm of GAP-43-deficient mice: association with midline recrossing and lack of normal ipsilateral axon turning. J Neurosci. 1998; 18: 10502-10513. PMID: 9852588
Neve RL, Coopersmith R, McPhie DL, Santeufemio C, Pratt KG, Murphy CJ, et al. The neuronal growth-associated protein GAP-43 interacts with rabaptin-5 and participates in endocytosis. J Neurosci. 1998; 18: 7757-7767. PMID: 9742146
Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997; 20: 84-91. PMID: 9023877
Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci. 2005; 21(1): 1-14. https://doi.org/10.1111/j.1460-9568.2004.03813.x PMID: 15654838
Dehmelt L, Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol. 2005; 6: 204. https://doi.org/10.1186/gb-2004-6-1-204 PMID: 15642108
Urbanska M, Blazejczyk M, Jaworski J. Molecular basis of dendritic arborization. Acta Neurobiol Exp (Wars). 2008; 68: 264-288.
Gardiner J, Overall R, Marc J. The microtubule cytoskeleton acts as a key downstream effector of neurotransmitter signaling. Synapse. 2011; 65: 249-256. https://doi.org/10.1002/syn.20841 PMID: 20687109
Brewster AL, Lugo JN, Patil VV, Lee WL, Qian Y, Vanegas F, et al. Rapamycin reverses status epilepticus-induced memory deficits and dendritic damage. PLOS One.2013; 8: e57808. https://doi.org/10.1371/journal.pone.0057808 PMID: 23536771
Dachet F, Bagla S, Keren-Aviram G, Morton A, Balan K, Saadat L, et al: Predicting novel histopathological microlesions in human epileptic brain through transcriptional clustering. Brain. 2015; 138: 356-370. https://doi.org/10.1093/brain/awu350 PMID: 25516101
Piorkowska K, Thompson J, Nygard K, Matushewski B, Hammond R, Richardson B. Synaptic development and neuronal myelination are altered with growth restriction in fetal guinea pigs. Dev Neurosci. 2014; 36(6): 465-476. https://doi.org/10.1159/000363696 PMID: 25277216
Eastwood SL, Weickert CS, Webster MJ, Herman MM, Kleinman JE, Harrison PJ. Synaptophysin protein and mRNA expression in the human hippocampal formation from birth to old age. Hippocampus. 2006; 16(8): 645-654. https://doi.org/10.1002/hipo.20194 PMID: 16807900
Eastwood SL, Burnet PW, McDonald B, Clinton J, Harrison PJ. Synaptophysin gene expression in human brain: a quantitative in situ hybridization and immunocytochemical study. Neuroscience. 1994; 59: 881-892. PMID: 8058126
Tarsa L, Goda Y. Synaptophysin regulates activity-dependent synapse formation in cultured hippocampal neurons. Proc Natl Acad Sci USA.2002; 99: 1012-1016. https://doi.org/10.1073/pnas.022575999 PMID: 11792847
Calhoun ME, Jucker M, Martin LJ, Thinakaran G, Price DL, Mouton PR. Comparative evaluation of synaptophysin-based methods for quantification of synapses. J Neurocytol. 1996; 25 (12): 821-828. PMID: 9023727
Deller T, Korte M, Chabanis S, Drakew A, Schwegler H, Stefanie GG, et al: Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. Proc Nat Acad Sci USA. 2003; 100: 10494-10499. https://doi.org/10.1073/pnas.1832384100 PMID: 12928494
Deller T, Merten T, Roth SU, Mundel P, Frotscher M. Actin-associated protein synaptopodin in the rat hippocampal formation: localization in the spine neck and close association with the spine apparatus of principal neurons. J Comp Neurol. 2000; 418: 164-181. PMID: 10701442
Asanuma K, Kim K, Oh J, Giardino L, Chabanis S, Faul C, et al: Synaptopodin regulates the actin-bundling activity of a-actininin anisoform-specific manner. J Clin Invest. 2005; 115: 1188-1198. https://doi.org/10.1172/JCI23371 PMID: 15841212
Okubo-Suzuki R, Okada D, Sekiguchi M, Inokuchi K. Synaptopodin maintains the neural activity-dependent enlargement of dendritic spines in hippocampal neurons. J Mol Cell Neurosci. 2008; 38: 266-276.
Held S, Mendl M, Devereux C, Byrne RW. Social tactics of pigs in a competitive foraging task: the 'informed forager' paradigm. Anim Behav. 2000; 59(3): 569-576. https://doi.org/10.1006/anbe.1999. 1322 PMID: 10715179
Hirayama H, Kurimoto T, Wada S, Machida N, Shikuma H, Shoji S, Horibe M. Antiepileptic effects of globulin-N, an intact human immunoglobulin and its tissue-distribution in kindled cats. Int J Clin Pharm. 1986; 24(3): 109-122.
Villani F, Avanzini G. The use ofimmunoglobulins in the treatment of human epilepsy. Neurol Sci.2002; 23 Suppl 1:S33-S37.
Pammi M, Weisman LE. Late-onset sepsis in preterm infants: update on strategies for therapy and prevention. Expert Rev Anti Infect Ther. 2015; 13(4): 487-504. https://doi.org/10.1586/14787210.2015. 1008450 PMID: 25661566
Ohlsson A, Lacy JB. Intravenous immunoglobulin for preventing infection in preterm and/or low birth weight infants. Cochrane Database Syst Rev.2013; 7: CD000361.
