Erythropoietin and Enriched Housing in Marlau™ Cages Protect Neurons and Cognitive Function in Epileptic Rats Raafat P

Erythropoietin and enriched housing in Marlau™ cages protect neurons and cognitive function in epileptic rats Raafat P. Fares

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Raafat P. Fares. Erythropoietin and enriched housing in Marlau™ cages protect neurons and cognitive function in epileptic rats. Human health and pathology. Université Claude Bernard - Lyon I, 2009. English. NNT : 2009LYO10343. tel-00608109

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UNIVERSITE CLAUDE BERNARD - LYON 1

Président de l’Université M. le Professeur L. Collet

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To Doctor Laurent BEZIN

I would like to thank in vivo

I dedicate this thesis to my family who supported me from Beyrouth

To my mother Fatmé, To my father Abdel Rassoul, To my brothers Ramzi, Rami, Rachad, Amir and to my uncle Youssef,

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Published Articles PNAS J Comp Neurol J Neurochem

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TABLE CONTENTS

Commonly used abbreviations ...... 17 Introduction...... 19 Review of the Literature...... 23 Part I. Epilepsy...... 25 I.1. Definition, frequency, prognosis and causes ...... 25 I.1.a Definition...... 25 I.1.b Frequency and prognosis...... 25 I.1.c Causes of epilepsy...... 25 I.2. Cognitive impairments and psychological disorders in people with epilepsy ...... 26 I.2.a Psychopathology, anxiety and depression...... 26 I.2.b Cognitive dysfunction...... 26 I.3. Neuroprotective strategies as potential therapeutic interventions in people with epilepsy28 I.3.a Epilepsy and neuronal loss...... 28 I.3.b Status epilepticus, epileptogenesis and epilepsy...... 29 I.3.c Neuroprotective strategies for preventing epilepsy...... 30 Part II. Erythropoietin ...... 31 II.1. Neuroprotective effects of Erythropoietin (Epo) ...... 31 II.2. rhEpo administration before SE...... 32 II.3. rhEpo administration after SE...... 33 II.4. Effect of rhEpo on cognition in normal animals...... 34 II.5. Effect of rhEpo on cognition in lesioned animals ...... 34 II.6. Mechanisms of Epo-mediated neuroprotection...... 35 II.7. Constitutive expression of EpoR in the brain...... 37 II.8. Induced brain expression of EpoR following brain insult and in brain disease...... 37 Part III. Environmental enrichment ...... 38 III.1. A starter for enrichment...... 38 III.1.a The birth of enrichment concept...... 38 III.1.b The craze for enrichment...... 38 III.1.c The current constituent of enrichment ...... 39 III.1.d Relevance to standardize enriched housing ...... 40 III.1.e Potential recommendations for an optimal enrichment program ...... 40 III.2. Enrichment induced brain plasticity ...... 45 III.2.a Morphology and anatomy...... 45 III.2.b Neurogenesis ...... 45 III.2.c Learning and memory...... 46 III.2.d Anxiety-like behavior...... 46 III.2.e Long Term Potentiation (LTP) ...... 47 III.2.f Neurotransmitters...... 47 III.2.g Neurotransmitters receptors...... 49 III.2.h Cellular and molecular basis of enrichment-induced neuroplasticity ...... 50 III.2.i Neurotrophic and growth factors...... 51 III.3. Enrichment and seizures...... 52 III.3.a Enrichment as a prevention tool against epileptogenesis...... 52 III.3.b Enrichment as a rehabilitation tool after chemically-induced SE...... 54 III. 4. Enrichment and other models of brain impairment...... 54 Results...... 57 Results - Part I...... 59

Results - Part II ...... 95 Results - Part III...... 119 General Discussion...... 141 Part I. Development of behavioral tools to improve standardization ...... 143 I.1. Development of the Marlau™ cage ...... 143 I.2. Development of the Water Exploration Test...... 144 Part II. Decreased vulnerability of the neuronal entity...... 145 II.1. Activation of EpoR gene expression in the VLR by repeated hypoxic exposures...... 145 II.2. Activation of EPO and EpoR gene expression in the VLR by environmental enrichment...... 145 II.3. Ubiquitous upregultion of EpoR gene expression after repeated hypoxic exposures when housed in Marlau™ cages...... 146 II.4. Neuroprotection by rhEpo in the VLR following elevated EpoR gene expression...... 147 Part III. Functional neuroprotection...... 147 III.1. Preserved spatial learning performances in epileptic rats housed in Marlau™ cages: towards an adaptative process...... 148 III.2. Persistence of anxiety-trait in epileptic rats housed in Marlau™ cages: can it be considered as an adaptive process?...... 149 III.3. rhEpo provided functional protection in epileptic rats reared in standard cages but not in Marlau™ cages ...... 150 Part IV. Seizure development ...... 152 Part V. Ending suggestions ...... 152 Part VI. Suggested perspectives in the short term...... 154 Reference List (n=310)...... 155

Commonly used abbreviations

Specific aims of the Thesis

I.1.a Definition.

I.1.b Frequency and prognosis.

I.1.c Causes of epilepsy.

I.2.a Psychopathology, anxiety and depression. .

I.2.b Cognitive dysfunction.

of seizure types, cognitive impairment arising from seizure activity can be reduced or reversed by effective seizure control (McCagh J, 2009). However, in seizures difficult to control, administration of a multiplicity of anti-epileptic drugs at high doses can be associated with or exacerbate cognitive impairments and psychological problems (see table 1). Finally, seizures or the side effects of anti-epileptic drugs may not be the only causes of cognitive dysfunction in people with epilepsy. Indeed, cognitive dysfunction has been demonstrated to precede the onset of diagnosed seizures in groups of children, who showed impaired attention, reaction time, location learning, executive function, language, psychomotor speed and academic skills. In addition, children with epilepsy who had academic difficulties prior to seizure onset were particularly at risk of cognitive impairment (Oostrom KJ, 2003; Hermann B, 2006).

Table 1: Side effects of Anti-epileptic drugs administration on cognition and behavior (Modified and adapated from the Book: Epilepsy by Simon Shorvon, ONL 2009). Drug Major putative mechanisms of action Side effects on cognition -Clobazam Enhances GABA action at the GABAergic receptors Behavioral and cognitive disturbances, personality and behavior -lonazepamam changes, hyperactivity, aggressiveness, withdrawal symptoms

-Phenobarbital Enhances GABA action at the benzodiazepine site at the Aggressiveness, cognitive dysfunction (memory and attentional GABAA receptor, inhibits glutamate excitability, weak effect on disturbances), paradoxial hyperkinesis and behavioral change -Primidone sodium, potassium, and calcium conductance in children Enhances GABAergic transmission at the GABA receptor by Psychosis, depression, word-finding difficulties and other Tiagabine A inhibiting GABA re-uptake cognitive effects, emotional lability Blocks conductance at the neuronal sodium channel, Cognitive dysfunction especially difficulties with memory, potentiates GABAergic inhibition at the GABAA receptor, Topiramate reduces excitatory actions of glutamate at AMPA receptor, attention, language and word finding, confusion, agitation, inhibits high-voltage calcium channels, inhibits carbonic amnesia, depression, anxiety, psychosis, emotional lability anhydrase Enhances GABAergic transmission by inhibiting the catabolic Vigabatrin enzyme gamma-aminobutyric acid transaminase (GABA-T), Psychosis, depression, confusion thereby increasing the synaptic concentration of GABA

Valproate Not fully understood. Action on GABA and glutaminergic Cognitive disturbance, aggressiveness, tremor, ataxia activity, calcium (T) conductance, and potassium conductance

Multiple actions including inhibition of sodium and T-type Attention and concentration difficulties, memory impairment, Zonisamide calcium currents, enhances GABAa receptor function, confusion, depression, mental slowing, speech disturbance, carbonic anhydrase inhibition, glutaminergic transmission aggressiveness, tremor, ataxia inhibition -Carbamazepine -Lamotrigine Effects on behavior and mood, depression, psychosis, Blocks conductance at the neuronal sodium channel movement disorder, anxiety, memory and attention defects, -Oxcarbazepine other cognitive, neurological and psychiatric effects -Phenytoin Enhances selectively slow inactivation at the neuronal sodium Lacosamide Depression, memory disturbance channel and modulates the action of the CMRP-2 protein Behavioral disturbances including aggression and irritability, Ethosuximide Inhibits neuronal T-type calcium channels hyperexcitability in children, acute psychotic reactions, depression Memory and attentional deficit, concentration difficulties, -Gabapentin Binds to the alpha2Theta subunit of the neuronal voltage- confusion and other cognitive effects, psychiatric disturbance, dependent calcium channel -Pregabalin depression, anxiety Behavioral change, irritability, aggression,mood change, Levetiracetam Binds to the synaptic vesicle protein SV2A depression, anxiety, psychosis, memory and attention disturbance

I.3.a Epilepsy and neuronal loss.

I.3.b Status epilepticus, epileptogenesis and epilepsy.

I.3.c Neuroprotective strategies for preventing epilepsy.

II.1. Neuroprotective effects of Erythropoietin (Epo)

II.2. rhEpo administration before SE

Table 2: rhEpo increases brain resistance to seizures and SE models rhEpo as a prevention tool SE & seizures Effects models

Female BALB/c mice -Delayed onset of SE Kainate Epo (5000 U/Kg; i.p, -Decreased mortality rate (~45%) 20 mg/Kg; i.p 24 hours prior to SE) -Increased survival time (~41%)

Brines ML, 2000 -Delayed onset of seizure Male Wistar rats Pentylentetrazol -Decreased severity of seizures Epo (3000 U/Kg; i.p, 80 mg/Kg; i.p -Decreased total seizure time 24 hours prior to SE) -Confined blood brain barrier leakage Uzum G, 2006 -Decreased seizure activity -Decreased TUNEL and levels of pro- Male Sprague Dawley rats Li-Pilocarpine apoptotic proteins (caspase-3, Bim and Bid) in the Epo (10 000U/Kg; i.p, 30 mg/Kg; i.p/s.c hippocampus 4 hours prior to SE) -Increased levels of anti-apoptotic proteins ( Bcl-w and Bcl-2) in the hippocampus Wen X, 2006; Yang J, 2007

Male Sprague Dawley rats Pilocarpine -Decreased number (-40%) of rats developing SE Epo (5000 U/Kg; i.p, 300 mg/Kg; i.p -Decreased number of stage 4/5 seizures 24 hours and 30 min prior to SE)

Nadam J, 2007

II.3. rhEpo administration after SE

Table 3: Beneficial effects of therapeutic administartion of rhEpo in SE models

rhEpo as a therapeutic tool SE model Effects

-Full protection of CA3 and SLMo Male Sprague Dawley rats Pilocarpine -Partial protection of Hilar interneurons, mossy Epo (5000 U/g; i.p, 300 mg/Kg; i.p cells and CA1pyramidal neurons 30min, 1 and 3 days post-SE) -No protection of ventral limbic region (VLR) Nadam J, 2007

Male Sprague Dawley rats 3 repeated hypoxia exposures Pilocarpine -As above plus protection of VLR Epo (5000 U/g; i.p, 300 mg/Kg; i.p 30min, 1 and 3 days post-SE)

Sanchez PE, 2009 -Cell protection in CA1,CA3 and the Hilus Male Sprague Dawley rats -Decreased blood brain barrier leakage Li-Pilocarpine Epo (5000 U/g; i.p, -Decreased number of rats developing convulsive repeated doses of Immediately after SE cessation and seizures 30 mg/Kg; i.p once daily for 7 days) -Decreased frequency and duration of hippocampal seizures Chu K, 2008

II.4. Effect of rhEpo on cognition in normal animals II.5. Effect of rhEpo on cognition in lesioned animals

Table 4 Brain injury model Study details

Epo: 1000U/Kg administered i.p after oxygenation in Wistar rats at P7 Test: MWM Kurmal A, 2004 Hypoxia-Ischemia Epo: 2500U/Kg administered s.c after oxygenation for 3d in Sprague-Dawley rats at P7 Test: sensorimotor response Demers EJ, 2005 Epo: 2000U/Kg administered intraperitoneally in Wistar rats at P7 Test: Rota-Rod treadmill-Grip traction-Foot fault-Postural reflex and Limb placing Spandou E, 2005 Epo: 5U/day continuously infused in the lateral ventricle for 28d of 12w SH-SP rats Test: MWM Sadamoto Y, 1998 Epo: 2,5 to 25U/day infused for 7d in the lateral ventricle of gerbils Test: Passive avoidance task Sakanaka M, 1998 Epo: 0,5 to 25U immediately injected after restoration of blood flow in the lateral ventricle of adult gerbils Test: Passive avoidance task Ischemia Catania MA, 2002 Epo: 5000 or 10 000U/Kg administered i.p for 7d in Wistar rats starting 24h after artery occlusion Test: Corner and foot-fault Wang L, 2004 Darbepoetin Alfa: 10μg/Kg administered i.p 2h after onset artery occlusion in adult Sprague-Dawley (SD) rats Test: postural reflex and forelimb placing Belayev L, 2005 Epo: 5000U/Kg ip or 4,8 to 24U intranasaly 10 min after artery occlusion and 24h after reperfusion in SD rats Test: neurological score Yu YP, 2005 Controlled cortical injury Epo: 5000U/Kg administered i.p daily for 14d in adult Wistar rats Test: MWM Lu D, 2005 Closed head injury Epo: 5000 U/Kg administered i.p 1h and 24h after injury in Sabra mice Test: Neurological severity score and Object recognition Yatsiv I, 2005 Transection of Epo: 5000U/Kg administered i.p during the injury in adult Wistar rats fimbria-fornix Test: MWM and 8 arm-radial maze Mogensen J, 2004; Mala H, 2005 Glutamate Epo: 2,5U injected consecutively with glutamate in the lateral nucleus of Amygdala in adult Wistar rats excitotoxic injury Test: Open field and Trace fear conditioning Miu AC, 2004 II.6. Mechanisms of Epo-mediated neuroprotection.

Epo

EpoR

P JAK2 JAK2 P

EpoR activation

Figure 1: Signal pathways of EpoR Transcriptional factors PI3K NFkB STAT5 MAPK Genes IAP Neuroprotection Apoptosis

II.7. Constitutive expression of EpoR in the brain. II.8. Induced brain expression of EpoR following brain insult and in brain disease.

III.1.a The birth of enrichment concept. III.1.b The craze for enrichment

III.1.c The current constituent of enrichment

Laviola G 2008 Mora F 2007 Will B 2004 Frick KM 2003McNair K 2007 Faverjon S 2002 Figure 2:

III.1.d Relevance to standardize enriched housing III.1.e Potential recommendations for an optimal enrichment program

A1 D1

mm510 A2 D2 B1 E1 G1 G2

B2 B2 E2 C1 F1 C2 F2 Figure 3:

Table 5 Animals Program Enrichment design MWM

Author Strain Sex En Ctrl Begin at Length Type RW TNL RMP TYS CHE LBH CPT Result

Wolf M, 2008 Rat F 12 3-4 42w 40d C - - - + daily - - +

Holguin S, 2008 Rat M 2 1 4w ? C - - - + 2/w - - +

Zanardi A, 2007 Mice F 10 2 3w 2m C + - + + 2/w + + +

Fan Y, 2007 Gerbil M ? 3 2m 2m C + + - + 2/w - + +

Toscano CD, 2006 Mice M-F 6-8 1 3w 6m C + + - + 1/w - - +

Meshi D, 2006 Mice F 8 4 12w 6w C + + - + - - + +

Huang FL, 2006 Mice ? ? ? 3-5m 3w C + - - + 2/w - - +

Benett JC, 2006 Mice ? 5 5 23m 6w C + + - + daily - - +

Jankowski JL, 2005 Mice F 16 3-4 2m 6m C + + - + - - - +

Giza CC, 2005 Rat M 16-18 ? 3w 17d C - + + + daily - + +

Foley AG, 2005 Rat ? 30 15 25d 55d C + + + + daily - + +

Hellemans KG, 2005 Rat M 12 2 3w 12w C + - + + 2/w - + +

Schrijver NC, 2004 Rat M 3 3 3w 80d C - - + + 1/w - - +

Guilarte TR, 2003 Rat ? 8 1 3w 30d C + + + + 1/w - + +

Frick KM, 2003 Mice M-F 4 4 ? 23d 3h/d + - - + - - + +

Bredy TW, 2003 Rat ? 8 2 22d 50d 3h/d - - - + regularly - + +

Schrijver NC, 2002 Rat M 3 3 3w 80d C - - + + 1/w - - +

Faverjon S, 2002 Rat M 9 ? 3w 30d 4h/d + + + + 2/w - + +

Pham TM, 1999 Rat ? 8 1 22d 2m 4h/d + + + + daily - - +

Nilsson M, 1999 Rat F 6 1 10w 4-8m 4h/d - - + + 2/w - - +

Kempermann G, 1997 Mice F 12 4 3w 40d C + + - + - - - +

Galani R, 1997 Rat M 12 1 ? 30d 4h/d - - + + daily - + +

Falkenberg T, 1992 Rat M 6 1 50d 34d 4h/d ? ? ? ? ? ? ? +

Rat ? ? ? 15d 12d 4h/d ? ? ? ? ? ? ? + Paylor R, 1992 Table 5:

Animals: En/Ctrl, . Program: Begin at, ; length, ; Type, C; Enrichment design: RW, ; TNL, RMP TYS CHE LBHCPTMWM: Morris Water Maze result; , MFwdmC +-

Table 6 Animals Program Enrichment design MWM

Author Strain Sex En Ctrl Begin at Length Type RW TNL RMP TYS CHE LBH CPT Result

Mandolesi L, 2008 Rat M 10 2 3w 3m C + - + + 2/w - + -

Comeau W, 2008 Rat M-F 4-6 3-4 3w 3m C - - - + 1/w - - -

Cao X, 2008 Rat M 8 2 3w 8w C + + + + 1/w - + -

Wurm F, 2007 Rat M 6-8 4 10-12w 5-8w C - + - + 1/w - - -

Wang CA, 2007 Rat M 8-10 2-3 25d 2w C + - + + 3/w - - -

Miu AC, 2006 Rat M 5-7 3-4 adult 10w C - + - + 2/w - - -

Ciu M, 2006 Rat ? ? ? 3w 30d C + + + + 1/w - + -

Briones TL, 2006 Rat M 9 2 3-4m 2w C + + - + daily - - -

Briones TL, 2006b Rat M 9 2 3-4m 2w C + + - + daily - - -

Ueda S, 2005 Rat M 5 2 4w 4w C + - - + daily - - -

Martinez-Cue C, 2005 Mice M 8-10 2-3 22d 7w C + - + + - - + -

Leggio MG, 2005 Rat ? 10 2 3w 3w C + - + + 1/w - + -

Gobbo OL, 2005 Rat M 4 3-4 adult 10w C + + - + 1/w - + -

Gobbo OL, 2004 Rat M 4 3 adult 10w C + + - + 1/w - + -

Hicks RR, 2002 Rat M 6 1 3w 2w C - - - + 3/w - - -

Schneider JS, 2001 Rat M 8 1 25d 75d C - + - + 3/w - - -

Passineau MJ, 2001 Rat M ? 1 adult 11d C + + + + - - + -

Pursky GT, 2000 Mice F ? 4-5 21d 40d C - + + + daily - - -

Caston J, 1999 Mice ? ? 5 1d 3m C + + + - - - + -

Van Rijzingen IM, 1997 Rat M 6-7 2 2m 6w C - + + + 1/w - - -

Puurunen K, 1997 Rat ? 6-7 1 ? 1w C + + - + 1/w + + -

Boehm GW, 1996 Mice F 4-6 4-6 3w 9w C + - + - - - - -

Wainwright PE, 1993 Mice ? 12 1 3w 7w C - - + + 3/w ? ? - Table 6:

Animals: En/Ctrl, . Program: Begin at, ; length, ; Type, C; Enrichment design: RW, ; TNL, RMP TYS CHE LBHCPTMWM: Morris Water Maze result; , MFwdmC +-

Table 7 Animals Program Enrichment design BDNF data

Author Strain Sex En Ctrl Begin at Length Type RW TNL RMP TYS CHE LBH CPT LOC State TCN Result

Kondo M, 2008 Rat M-F 5-6 5-6 4w 10-26w C + - - + 3/w - - Hi Prot Elisa -

Segovia G, 2008 Rat M 10-12 1 3m 19m C + + - + 1/w - - Hi Prot Elisa -

Bindu B, 2007 Rat M 8-10 2-3 2m 10d 6h/d - + + + daily - - Hi Prot WB -

Rossi C, 2006 Mice 5-6 2-3 10w 8w C + + + + 1/w - - Hi Prot WB +

Zhu SW, 2006 MiceM663w4mC?????--HiProtWB+ (D-V)

Gobbo OL, 2004;5 Rat M 4 3-4 adult 10w C + + - + 1/w - + Hi Prot Elisa + (DG)

Gresack JE, 2004 Mice F ? ? 3w 7m 3h/d + - - + daily - - Hi Prot Elisa -

Spires TL, 2004 Mice ? ? ? 4w 4m C - + - + 3/w - - Hi Prot WB -

Guilarte TR, 2003 Rat ? 8 1 3w 4w C + + + + 1/w - + Hi mRNA IS-H -

Hicks RR, 2002 Rat M 6 1 3w 2w C - - - + 3/w - - Hi mRNA IS-H -

Schneider JS, 2001 Rat M 6 1 25d 10w C - + - + 3/w - - Hi mRNA RT-PCR + (D)

Zhao L, 2000 Rat M 8-10 4 3m 12-20d C - - - + 3/w - - CA2 mRNA IS-H -

Ickes B, 2000 Rat M 6 1 8w 12m C + + + + 2/w - - Hi Prot Elisa + (V)

Young D, 1999 Rat M 6 1 3w 3w C + + - + - - - Hi Prot Immuno + (MF)

Falkenberg T, 1992 Rat M ? 7w 7w 34d C ? ? ? ? ? ? ? Hi mRNA IS-H - (D) Table 7:

Animals: En/Ctrl, . Program: Begin at, ; length, ; Type, C; Enrichment design: RW, ; TNL, RMP TYS CHE LBHCPTBDNF data: LOC, ; State, ; TCN, M F w d m C + -

III.2.a Morphology and anatomy III.2.b Neurogenesis Enrichment protocol starting at weaning.

Enrichment protocol starting at 6 weeks or more. III.2.c Learning and memoryMorris water Maze (MWM). No effect Positif effect (49%) (51%)

Figure 4 Morris Water Maze III.2.d Anxiety-like behavior Elevated Plus Maze (EPM).

III.2.e Long Term Potentiation (LTP) III.2.f Neurotransmitters GABA and its synthesis enzyme glutamate decarboxylase (GAD).

Glutamate. Acetylcholine ACh and its synthesis enzyme “choline acetyltransferase” (ChAT). Dopamine and its transporter DAT. Noradrenaline (NA) and serotonin (5-HT).

III.2.g Neurotransmitters receptors 5-HT receptors. Dopamine receptors. GABA receptor. Ionic glutamate receptors (AMPA). Ionic glutamate receptors (NMDA). Metabotropic glutamate receptors.

III.2.h Cellular and molecular basis of enrichment-induced neuroplasticity Immediate Early Gene (IEG). Zif268 Krox-20. NGFI-B. Arc. Large scale analysis of transcriptomic and proteomic alterations.

III.2.i Neurotrophic and growth factors BDNF in the hippocampus. BDNF in other brain regions.

Other factors. NGF GDNF. NT-3 IGF-1. VEGF.

III.3.a Enrichment as a prevention tool against epileptogenesis

Enriched environment tested as a prevention tool in SE models

Isolated housing -Analysis of SE At 3w 3weeks later Parameters -Cell death induced by SE

Enriched housing Kainic acid Young D, 1999 (8;10;12 mg/kg)

Isolated housing -Number of stimulations for At 6w 4weeks later Parameters each behavioral stage

Enriched housing Amygdala kindling Auvergne R, 2002

III.3.b Enrichment as a rehabilitation tool after chemically-induced SE

Enriched environment tested as a rehabilitation tool in SE models

Isolated housing -Cognitive function (MWM) At P20 Intermittent (4h/d) or continuous (4w) Parameters -Cell death induced by SE -Seizure threshold at adult age Pilo Enriched housing (60mg/kg) Rutten A, 2002; Faverjon S, 2002; Wang CA, 2007

Isolated housing -Exploratory behavior (Open field test) At P20-25 10 to 14 days later Parameters -Depressive behavior (Porsolt test) -Gene expression Kainic acid Enriched housing (10mg/kg) Koh S 2005; Koh S 2007

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SE (Li/Pilo) at day 22 (3 weeks) rEpo from P22 to P26 (5 injections, 5000 IU/kg each) Standard Housing (SH) or Enriched Housing (EH) at day 23

A B Weeks (post-SE) 2 1213 15 24 26 C/SH (n=10) 2 5 Age (weeks) 5 15 16 18 27 29 C/EH (n=12) 1 12 Test WET WET MWM EPM Retention End Test SE/SH (n=8) 2 4 SE/EH (n=8) 1 8 ! 1-5 w. post-SE SE/rEpo/SH (n=9) 2 4-5 Watch for SE/rEpo/EH (n=9) 1 9 1st BSRS

Figure 1. Experimental design of behavioral studies. Anxiety and cognitive performances were assessed longitudinally in rats from 5 to 27 weeks of age. Rats were distributed in 6 groups, reared in standard (SH) or enriched (EH) housing from day 23 and throughout the experiment. The number of cages in which the “n” rats were distributed in each group (A), and the number of animals per cage (B) is provided. After Li/Pilo- SE at P22, half of rats received daily rEpo injections for 5 consecutive days, and were reared either in standard (SE/rEpo/SH) or in enriched (SE/rEpo/EH) cages, while the other half received saline injections instead of rEpo (SE/SH and SE/EH). Control rats receiving saline only were also added to the experiment (C/SH and C/EH). Abbreviations: BSRS, behavioral spontaneous recurrent seizures; C/EH, control rats in enriched Marlau™ cages ; C/SH, control rats in standard cages; EPM, Elevated Plus Maze; MWM, Morris Water Maze; SE/EH, rats subjected to SE and reared in enriched Marlau™ cages; SE/rEpo/EH, rats subjected to SE, treated with rEpo and reared in enriched Marlau™ cages; SE/SH, rats subjected to SE and reared in standard cages; SE/rEpo/SH, rats subjected to SE, treated with rEpo and reared in standard cages; WET, Water Exploration Test. 100% Rats developing SE

80%

60%

40%

20% Rats surviving SE 0 Pilo (mg/kg) 15 20 25 30 40

Figure 2. Effect of pilocarpine dose on status epilepticus development and survival in young rats. Lithium (3 mEq/kg, i.p.) was administered at day 21, 18 hours prior to pilocarpine. Among the five doses of pilocarpine tested at day 22, 25mg/kg was the optimal dose to induce a sustained SE in high number of rats with minimal death rate compared to other doses. A. Fluoro-Jade B : 24 hrs post-SE NCx CA1 Hilus ThD BLA

B. NeuN : 2 weeks post-SE C. Hilus : 2 weeks post-SE C - Hilus C - BLA SOM CGRP

SE - Hilus SE - BLA SOM-IR cell # CGRP-IR cell # 120 120 90 90 60 60 30 30 0 0 CSE CSE

Figure 3. Lack of evidence of massive neurodegenerative processes following pilocarpine induced SE in young rats. A. Fluora-Jade B staining, which is a marker of neuronal degeneration, was observed 24hours post-SE (at day 23) in several brain regions. B. Two weeks post-SE, no obvious neuronal loss was observed in the brain, notably in the Hilus and the BLA using the neuronal marker NeuN. C. Counting hilar neurons using SOM and CGRP markers showed no difference between controls and rats subjected to SE two weeks earlier. Abbreviations: BLA, basolateral nucleus of the amygdala; C, controls; CGRP, calcitonin gene-related peptide; IR, immunoreactive; NCx, Neocortex; ThD, dorsal part of the thalamus; SE, status epilepticus; SOM, somatostatin. Epo-mRNA EpoR-mRNA in percent of « C » in percent of « C »

HiD a 300

200 100

0 NCx 300 a a a a 200 100

0 ThD 300

200 a

100 a a a 0 VLR 300

200

100 a

0 C 10h 24h 72h C 10h 24h 72h post-SE post-SE

Figure 4. Brain expression profile of Epo/EpoR system following SE. Transcripts encoding Epo and EpoR were quantified using RT-qPCR in the dosal hippocampus (HiD), the neocortex (NCx), the dorsal part of the thalamus (ThD) and the basolateral nucleus of the amygdala (BLA) following SE induced at P22 by pilocarpine. All values were normalized against the SmRNA, as explained in Materials and Methods. Abbreviations: C, controls; HiD, dorsal hippocampus; NCx, Neocortex; ThD, dorsal part of the thalamus; VLR, ventral limbic region; SE, status epilepticus. a: p<0.05 compared to C, Fisher’s LSD test following ANONA1. 5 weeks post-SE 100% SH EH

80%

60%

Rats with BSRS 40%

20%

0 SE ++ ++ rEpo - + - +

Figure 5. Percentage of rats with BSRS monitored during the 5 weeks following SE. BSRS, when occurred, appeared within the 4th week after Li/Pilo-SE. Abbreviations: SH, standard housing; EH, enriched housing. WET: 2 weeks post-SE 25% SH EH a 20%

b 15% b

b 10% b

Time in the central zone 5%

0 SE -++ -++ rEpo --+ --+

Figure 6. Anxiety increases in all rats prior to BSRS, independently of the housing conditions and rEpo treatment. Performances of all rats were measured in the WET two weeks after SE. In this test, the more time rats spend in the central zone, the less anxious they are considered. Group explanations are given in figure 1. Control rats reared in EH had a less anxious profile than those reared in SH. SE increased anxiety-trait in both housing conditions, and rEpo had no effect. a: p<0.05, control EH vs. control SH; b: p<0.05, vs. respective SH or EH controls; Fisher’s LSD test following ANOVA2. Abbreviations: SE, status epilepticus; SH, standard housing; EH, enriched housing. WET: 12 weeks post-SE Time in the central zone Swimming profile SH EH EH 40% a 40% Time in the central zone at :

b Null Rapid velocity 30% 30% velocity c

b,c 20% 20%

b 10% 10% c

0 SE -++ -++ ++ ++ rEpo --+ --+ - + - +

Figure 7. At 12 weeks post-SE, rEpo increased anxiety-like behavior in rats with BSRS reared in enriched but not in standard housing At 15 weeks of age (12 weeks post-SE), anxiety-like behavior was assessed in control rats and rats with BSRS using the WET. In this test, the more time rats spend in the central zone, the less anxious they are considered. Rats with BSRS in SH and EH groups were more anxious than their respective controls. In addition, rEpo administered after SE exacerbated anxiety in rats with BSRS, as shown by the decreased time spent in the central zone and the significant alteration of the swimming profile (decreased floating behavior, i.e. null velocity, and increased rapid velocity). a: p<0.05, control EH vs. control SH; b: p<0.05, vs. respective SH or EH controls; c: p<0.05, vs. SE without rEpo; Fisher’s LSD test following ANOVA2. Abbreviations: EH, enriched housing; SE, status epilepticus; SH, standard housing. EPM: 15 weeks post-SE Number of entries in OA Time in OA (in sec)

12 SH EH 70 SH EH a a 10 60 50 8 b 40 6 b,c c 30 c b,c 4 20 b 2 10 b 0 0 -++ -++ SE -++ -++ --+ --+ rEpo --+ --+

Figure 8. At 15 weeks post-SE, rEpo exerts opposite effects on anxiety in the EPM in rats reared in SH compared to EH. At 18 weeks of age (15 weeks post-SE), anxiety was assessed in rats using the EPM. In this test, the more rats enter and spend time in the open arm (OA), the less anxious they are considered. All rats with BSRS exhibited a highly anxious profile, which was almost completely recovered and exacerbated by rEpo administration when rats were reared in SH and EH, respectively. a: p<0.05, control EH vs. control SH; b: p<0.05, vs. respective SH or EH controls; c: p<0.05, vs. SE without rEpo; Fisher’s LSD test following ANOVA2. Abbreviations: EH, enriched housing; SE, status epilepticus; SH, standard housing. MWM: 13 weeks post-SE A : Latency to platform in sec 100 100 a,b a,b SE/SH 80 80 a,b SE/EH 60 SE/rEpo/SH 60

40 40 C/SH C/EH 20 20 SE/rEpo/EH SH EH 0 0 D1 D2 D3 D4 Days D1 D2 D3 D4 Days

B: Percent of platform finders 120 120 SH EH 100 100

80 80

60 60

40 40

20 20

0 0 -++ -++ SE -++ -++ --+ --+ rEpo --+ --+ Day 1 Day 4 Day 1 Day 4

Figure 9. At 13 weeks post-SE, rEpo protects rats with BSRS from learning impairment in MWM when reared in SH. At 16 weeks of age (13 weeks post-SE), learning was assessed in the MWM in control rats and rats with BSRS developed after SE. The upper graph represents the latency to find the platform from days 1 to 4, while the lower graph shows the percent of rats that found the platform on days 1 and 4. Only rats with BSRS reared in SH exhibited a severe cognitive impairment compared to controls. rEpo administration completely abolished the development of this cognitive decline. Note that rats with BSRS reared in EH were completely protected with no additional effect of rEpo. a: p<0.05, C/SH vs. SE/SH; b: p<0.05, SE/rEpo/SH vs. SE/SH; Fisher’s LSD test following ANOVA2 with repeated measures. Abbreviations: EH, enriched housing; SE, status epilepticus; SH, standard housing. Retention test: 24 weeks post-SE

SH EH 100%

80%

60%

Platform finders 40%

20%

0 SE ++ ++ rEpo - + - +

Figure 10. At 24 weeks post-SE, rEpo exerts opposite effects on spatial memory retention in rats reared in SH compared to EH. Eleven weeks after the achievement of the MWM test, we tested whether rats with BSRS that did find the platform at the 4th trial day (see fig. 8B) could find it again in a three-trial session. Rats were considered as “platform finders” when they found the platform in 2 consecutive trials. When reared in EH, all rats with BSRS not treated with rEpo remembered the position of the platform. However, rEpo treatment abolished this effect. By contrast, rEpo administered to rats with BSRS reared in SH improved memory retention. Abbreviations: EH, enriched housing; SE, status epilepticus; SH, standard housing. A. NeuN SE/EH - Hi SE/EH - NCx

SE/rEpo/EH - Hi SE/rEpo/EH - NCx

B. Hilar neurons SOM-IR cell # CGRP-IR cell # 100 SH EH 100 SH EH 80 80

60 60 40 40

20 20 0 0 ++ ++ SE ++ ++ - + - + rEpo - + - +

Figure 11. Administration of rEpo post-SE increased cerebral vascularity in rats with BSRS, only when reared in EH. At 29 weeks of age, all rats were sacrificed for histological analysis. A. While no neuron loss was noted following NeuN staining at this age in rats with BSRS, an important increase in blood vessel (see arrows) density was observed in rats (n=3/6) treated with rEpo and reared in EH compared to rats not treated with rEpo. B. No difference in the number of SOM-IR and CGRP-IR neurons was found in the hilus of rats raised either in SH or EH conditions, and treated or not with rEpo. Abbreviations: CGRP, calcitonin gene-related peptide; EH, enriched housing; Hi, hippocampus; IR, immunoreactive; NCx, neocortex; SE, status epilepticus; SH, standard housing; SOM, somatostatin.

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Reference List (n=310)

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