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Molecular, Cellular, and Behavioural Effects Produced by Perinatal Asphyxia: Protection by Poly (ADP-Ribose) Polymerase 1 (PARP-1) Inhibition

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Handbook of Neurotoxicity

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Abstract

Perinatal asphyxia implies oxygen interruption at birth, leading to death whenever reoxygenation is not promptly reestablished. Reoxygenation triggers a cascade of biochemical events for restoring function at the cost of improper homeostasis. The effects observed long after perinatal asphyxia have been explained by overexpression of sentinel proteins, such as poly(ADP-ribose) polymerase 1 (PARP-1), competing for NAD+ during reoxygenation, leading to the idea that sentinel protein inhibition constitutes a suitable therapeutic strategy. Asphyxia also induces transcriptional activation of proinflammatory factors, including NFκB, and its subunit p65, whose translocation to the nucleus was found here, is significantly increased in brain tissue from asphyxia-exposed animals, in tandem with PARP-1 overactivation, suggesting that PARP-1 inhibition downregulates the expression of proinflammatory cytokines. Indeed, TNF-α and IL-1β were found to be increased 8 and 24 h after perinatal asphyxia in mesencephalon and hippocampus of rat neonates.

The possible neuroprotection effect of nicotinamide has been studied in an experimental model of global perinatal asphyxia in rats, inducing the insult by immersing rat fetuses into a water bath for various periods of time. Following asphyxia, the pups are delivered, immediately treated, or given to surrogate dams for nursing, pending further experiments. Systemic administration of nicotinamide was found to rapidly distribute into the brain reaching a steady-state concentration sufficient to inhibit PARP-1 activity for several hours. Nicotinamide prevented several of the long-term consequences elicited by perinatal asphyxia, supporting the idea that it constitutes a lead for exploring compounds with similar or better pharmacological profiles.

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Abbreviations

AIF:

Apoptosis-inducing factor

AN:

Nicotinamide-treated, asphyxia-exposed rats

AS:

Asphyxia exposed, saline treated

ATP:

Adenosine triphosphate

BAD:

Bcl-2-associated death factor

BAX:

Bcl-2-associated X factor

BBB:

Blood–brain barrier

bFGF:

Basic fibroblast growth factor

CNS:

Central nervous system

COX-2:

Cyclooxygenase-2

CREB:

cAMP-response element-binding protein

CS:

Caesarean delivered, saline treated

DG:

Dentate gyros

DNMT1:

DNA(cytosine-5-)-methyl transferase 1

DPQ:

3,4-dihydro-5-[4-(1-piperidinyl)butoxy]-1(2H)-isoquinolinone

DR2313:

2-methyl-3,5,7,8-tetrahydrothiopyranol[4,3-d]pyrimidine-4-one

E2F:

Family of DNA-binding transcription factors

EPO:

Erythropoietin

ERCC2:

Excision repair cross-complementing rodent repair group 2

ERK:

Extracellular signal-regulated kinases

FOXO:

Subclass of forkhead O family of transcription factors

FR247304:

5-Chloro-2-[3-(4-phenyl-3,6-dihydro-1(2H)-pyridinyl) propyl]-4(3H)-quinazoline

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

HDAC:

Histone deacetylases

HIF:

Hypoxia-inducible factor

HRE:

Hypoxia-responsive elements

ICAM-1:

Intercellular adhesion molecule-1

IGF-1:

Insulin-like growth factor-1

IL-1β:

Interleukin-1β

iNOS:

Inducible nitric oxide synthase

IQ:

Intelligence quotient

IκB:

Inhibitor of kappa B protein

Ku70:

Protein encoded by the XRCC1 gene, required for the nonhomologous end joining pathway of DNA repair

LIG3:

DNA ligase 3

LPS:

Lipopolysaccharides

NAD+:

Nicotinamide adenine dinucleotide

NADH:

Reduced nicotinamide adenine dinucleotide

NFκB:

Nuclear factor-κB

ONO-1924H:

N-3-(4-oxo-3,4-dihydrophthalazin-1-yl)phenyl-4-(morpholin-4-yl) butanamide methane sulfonate monohydrate

P:

Postnatal day

p300:

Histone acetyltransferase p300

p65:

Transcription factor p65

PAR:

Poly(ADP-ribose) polymers

PARG:

Poly(ADP-ribose) glycohydrolase

PARPs:

Poly(ADP-ribose) polymerases

PARylated PARP:

Poly-ADP-ribosylated PARP

PBS:

Phosphate-buffered saline

PCAF:

P300/CBP-associated factor

PCr:

Phosphocreatine

PHD:

Prolyl hydroxylase domain

PJ34:

[N-(6-oxo-5,6-dihydrophenanthridin-2-yL)-N,N-dimethylacetamide.HCl]

POLB, DNA:

Polymerase-β

ROS:

Reactive oxygen species

SIRT:

Sirtuin

SRY:

Sex-determining region Y

Strep-HRP:

Streptavidin-horseradish peroxidase

SVZ:

Subventricular zone

TH:

Tyrosine hydroxylase

TNF:

Tumor necrosis factor

TUNEL:

Terminal deoxynucleotidyl transferase dUTP nick end labelling

VEGF:

Vascular endothelial factor

XRCC1:

X-ray cross-complementing factor 1

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Acknowledgments

Contract grant sponsors: FONDECYT-Chile (contracts: 1120079; 1110263; 1120577) (MH-M; PM; MH), CONICYT/DAAD (contract: 1378–090529) (PJG-H; MH-M), Millennium Institute Initiative-Chile (BNI P09-015-F), BMBF (NGFN+ TP9), and DAAD (415/alechile) (PJ G-H). TN-P and VM are MECESUP (UCH0704) fellows; PE-M and ER-M are CONYCYT fellows. The excellent technical from Mr. Juan Santibañez and Ms. Carmen Almeyda is acknowledged.

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Authors and Affiliations

  1. Millennium Institute BNI-Chile, Program of Molecular and Clinical Pharmacology, ICBM, BNI, Medical Faculty, University of Chile, Santiago, Chile

    T. Neira-Peña, P. Espina-Marchant, E. Rojas-Mancilla, D. Esmar, C. Kraus, V. Munoz, R. Perez, B. Rivera, D. Bustamante, J. L. Valdes, M. Hermoso, P. Gebicke-Haerter, P. Morales & M. Herrera-Marschitz

  2. Department of Psychopharmacology, Central Institute of Mental Health, Mannheim, Germany

    P. Gebicke-Haerter

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  14. M. Herrera-Marschitz
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Correspondence to M. Herrera-Marschitz .

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  1. Department of Biomedical Sciences, Quillen College of Medicine East Tennessee State University, Johnson City, TN, USA

    Richard M. Kostrzewa

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Neira-Peña, T. et al. (2022). Molecular, Cellular, and Behavioural Effects Produced by Perinatal Asphyxia: Protection by Poly (ADP-Ribose) Polymerase 1 (PARP-1) Inhibition. In: Kostrzewa, R.M. (eds) Handbook of Neurotoxicity. Springer, Cham. https://doi.org/10.1007/978-3-031-15080-7_115

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