O laboratorio Villapol estuda os mecanismos inflamatorios e neurodexenerativos desencadeados despois das lesións cerebrais, ou en enfermidades neurodexenerativas coma o alzhéimer.

Tamén estuda a conexión do cerebro coa microbiota intestinal, as aplicacións da nanomedicina terapéutica no cerebro, ou os efectos neurolóxicos a curto ou longo prazo nos pacientes con Covid-19.

 

Contribucións á ciencia

1. Lesión cerebral neonatal, neuroinflamación e vías apoptóticas. Durante o meu doutoramento en neurociencia estudei os mecanismos da neuroinflamación e da morte neuronal nun modelo de excitotoxicidade mediante a inxección de NMDA no cerebro neonatal de roedores. Estudiei as diferencias entre o cerebro adulto e neonatal e os mecanismos de neurodexeneración independentes e as diferencias de xénero. A activación da microglía/macrófagos, a astrogliose e as diferentes vías apoptóticas foron os meus campos de investigación desde 2003 ata o 2007. Estes descubrimentos levaron a dúas publicacións de primeira autora e catro de coautora. Ao estudar os mecanismos do dano cerebral, tiven a oportunidade de desenvolver un amplo conxunto de habilidades e unha base sólida para iniciar a miña carreira investigadora.

2. Isquemia cerebral en neonatos e tratamentos. Despois de completar o meu doutoramento, o goberno francés concedeume unha bolsa de investigación altamente competitiva, "Research in Paris", que me permitiu iniciar a miña formación posdoutoral no ano 2007. Aprendín o complexo modelo de isquemia cerebral neonatal das mans do seu creador, o Dr. Sylvain Renolleau (Modelo isquémico Renolleau) e da miña mentora, a Dra. Christiane Charriaut-Marlangue. Estudei tratamentos neuroprotectores en modelos animais que aplicamos ós recén nacidos prematuros con danos cerebrais. Explorei diferentes terapias nun modelo neonatal de ictus, incluíndo inhibidores endóxenos da apoptose (óxido nítrico, melatonina). O tratamento con melatonina púxose á práctica clínica en bebés prematuros con dano cerebral no hospital Robert Debré, onde tiña o meu laboratorio. A miña primeira etapa de formación posdoutoral en París foi moi productiva, publiquei tres traballos de primeiro autora e cinco máis coma coautora que abordaban os temas anteriores.

3. Neurorestauración despois da lesión cerebral traumática por bloqueo do receptor da angiotensina II. Comecei a miña segunda formación posdoutoral no Centro de Neurociencia e Medicina Rexenerativa e NIH (Bethesda, Maryland, EE.UU.) no 2010. Esta transición representou unha oportunidade para seguir investigando estratexias terapéuticas para o dano cerebral, pero cun foco claro no trauma cerebral. Comecei a estudar o tratamento dos bloqueadores dos receptores da anxiotensina nun modelo de rato de dano cerebral. O meu traballo publicouse en revistas de alto impacto. Estes estudos publicáronse en seis artigos de primeira autora e cinco máis coma coautora. Ademais, supervisei e co-tutorei a un total de doce membros de laboratorio con diferentes niveis de experiencia (estudiantes de grao, máster, doutoramento e técnicos de laboratorio).

4. Órganos periféricos e inflamación en reposta ao trauma cerebral. No 2014 incorporeime ao departamento de neurociencia da Universidade de Georgetown como profesora asistente de investigación. O meu tema de investigación centrouse principalmente en como os mediadores inflamatorios conectan o cerebro con órganos periféricos, coma o fígado, e como estes mecanismos dependen do sexo. No 2016, conseguín o meu primeiro proxecto de financiación do NIH que me axudou a establecer unha liña de investigación independente coma Investigadora Principal de inicio de carreira. O meu laboratorio explorou os mecanismos do eixe cerebro-intestino-microbioma en resposta ao trauma cerebral.

5. O eixe cerebro-periferia, cambios no microbioma, nanotecnoloxía para a entrega de fármacos despois da lesión cerebral. Establecei o meu laboratorio no Instituto de Investigación do Hospital Methodist, en Houston no ano 2018. O meu laboratorio céntrase en explorar coma o cerebro se comunica coa periferia a través das vías inflamatorias e neuroinmunes e buscando novos mecanismos de administración de medicamentos e tratamentos eficaces para o dano cerebral e as enfermidades neurodexenerativas. Interésame o eixe cerebro-intestino-microbioma e os biomarcadores en órganos periféricos. Ao estudar a inflamación e a dexeneración no cerebro utilizando varios modelos animais, tamén me interesei no proceso de devolver achados significativos do microbioma aos participantes na investigación. Dirixín unha investigación clínica que examinaba os cambios no microbioma intestinal en xogadores de fútbol despois dunha conmoción cerebral, e temos varias en pacientes con distintos tipos de lesión cerebaris. Outro proxecto céntrase na nano-neurotecnoloxía e na lesión cerebral para estudar os primeiros respondedores biolóxicos para identificar biomarcadores que respondan en segundos ao dano cerebral. Así, o meu futuro programa de investigación focalizase en buscar tratamentos para restaurar o cerebro danado e os procesos neurodexenerativos.

6. COVID-19. O noso grupo tamén investiga os cambios na microbiota dos pacientes hospitalizados da Covid e os seus efectos neurolóxicos na Covid a longo prazo.

PUBLICACIÓNS: (PubMed Search) (Google Scholar) (Research Gate)

I. Artigos Orixinais en Revistas de Referencia:

(Orde cronolóxica; 60 total) h-index: 30 i10-index: 49).

1.     A multinational Delphi consensus to end the COVID-19 public health threat. Lazarus JV, Romero D, Kopka CJ, Karim SA, Abu-Raddad LJ, Almeida G, Baptista-Leite R, Barocas JA, Barreto ML, Bar-Yam Y, Bassat Q, Batista C, Bazilian M, Chiou ST, Del Rio C, Dore GJ, Gao GF, Gostin LO, Hellard M, Jimenez JL, Kang G, Lee N, Matičič M, McKee M, Nsanzimana S, Oliu-Barton M, Pradelski B, Pyzik O, Rabin K, Raina S, Rashid SF, Rathe M, Saenz R, Singh S, Trock-Hempler M, Villapol S, Yap P, Binagwaho A, Kamarulzaman A, El-Mohandes A; COVID-19 Consensus Statement Panel.Nature. 2022 Nov;611(7935):332-345. doi: 10.1038/s41586-022-05398-2. Epub 2022 Nov 3.PMID: 36329272 Free PMC article.

2.     Emu: species-level microbial community profiling of full-length 16S rRNA Oxford Nanopore sequencing data.Curry KD, Wang Q, Nute MG, Tyshaieva A, Reeves E, Soriano S, Wu Q, Graeber E, Finzer P, Mendling W, Savidge T, Villapol S, Dilthey A, Treangen TJ.Nat Methods. 2022 Jul;19(7):845-853. doi: 10.1038/s41592-022-01520-4. Epub 2022 Jun 30.PMID: 35773532

3.     Long-COVID in children and adolescents: a systematic review and meta-analyses. Lopez-Leon S, Wegman-Ostrosky T, Ayuzo Del Valle NC, Perelman C, Sepulveda R, Rebolledo PA, Cuapio A, Villapol S.Sci Rep. 2022 Jun 23;12(1):9950. doi: 10.1038/s41598-022-13495-5.PMID: 35739136 Free PMC article.

4.     Vaccinate fast but leave no one behind: a call to action for COVID-19 vaccination in Spain.

Lazarus JV, Bassat Q, Crespo J, Fanjul G, Garcia-Basteiro AL, Hoyos ML, Mateos C, Gutierrez JM, Naniche D, Oliu-Barton M, Rabin KH, Vilasanjuan R, Villapol S, Martin-Moreno JM.Commun Med (Lond). 2021 Jul 7;1:12. doi: 10.1038/s43856-021-00014-2. eCollection 2021.PMID: 35602186 Free PMC article. 

5.     Fecal Microbiota Transplantation Derived from Alzheimer's Disease Mice Worsens Brain Trauma Outcomes in Wild-Type Controls. Soriano S, Curry K, Wang Q, Chow E, Treangen TJ, Villapol S.Int J Mol Sci. 2022 Apr 19;23(9):4476. doi: 10.3390/ijms23094476.PMID: 35562867 Free PMC article.

6.     Alterations to the gut microbiome after sport-related concussion in a collegiate football players cohort: A pilot study. Soriano S, Curry K, Sadrameli SS, Wang Q, Nute M, Reeves E, Kabir R, Wiese J, Criswell A, Schodrof S, Britz GW, Gadhia R, Podell K, Treangen T, Villapol S.Brain Behav Immun Health. 2022 Mar 1;21:100438. doi: 10.1016/j.bbih.2022.100438. eCollection 2022 May.PMID: 35284846 Free PMC article.

7.     Alterations to the gut microbiome after sport-related concussion in a collegiate football players cohort: A pilot study. Soriano S, Curry K, Sadrameli SS, Wang Q, Nute M, Reeves E, Kabir R, Wiese J, Criswell A, Schodrof S, Britz GW, Gadhia R, Podell K, Treangen T, Villapol S.Brain Behav Immun Health. 2022 Mar 1;21:100438. doi: 10.1016/j.bbih.2022.100438. eCollection 2022 May.PMID: 35284846 Free PMC article.

8.     A contemporary review of therapeutic and regenerative management of intracerebral hemorrhage. Sadaf H, Desai VR, Misra V, Golanov E, Hegde ML, Villapol S, Karmonik C, Regnier-Golanov A, Sayenko D, Horner PJ, Krencik R, Weng YL, Vahidy FS, Britz GW.Ann Clin Transl Neurol. 2021 Nov;8(11):2211-2221. doi: 10.1002/acn3.51443. Epub 2021 Oct 14.PMID: 34647437 Free PMC article. Review.

9.     Biomimetic Nanoparticles as a Theranostic Tool for Traumatic Brain Injury. Zinger A, Soriano S, Baudo G, De Rosa E, Taraballi F, Villapol S.Adv Funct Mater. 2021 Jul 23;31(30):2100722. doi: 10.1002/adfm.202100722. Epub 2021 Mar 26.PMID: 34413716 Free PMC article.

10.  More than 50 long-term effects of COVID-19: a systematic review and meta-analysis. Lopez-Leon S, Wegman-Ostrosky T, Perelman C, Sepulveda R, Rebolledo PA, Cuapio A, Villapol S.Sci Rep. 2021 Aug 9;11(1):16144. doi: 10.1038/s41598-021-95565-8.PMID: 34373540 Free PMC article.

11.  Natural tannin extracts supplementation for COVID-19 patients (TanCOVID): a structured summary of a study protocol for a randomized controlled trial. Molino S, Pisarevsky A, Mingorance FL, Vega P, Stefanolo JP, Repetti J, Ludueña G, Pepa P, Olmos JI, Fermepin MR, Uehara T, Villapol S, Savidge T, Treangen T, Viciani E, Castagnetti A, Piskorz MM.Trials. 2021 Apr 28;22(1):310. doi: 10.1186/s13063-021-05281-x.PMID: 33910614 Free PMC article.

12.  COVID-SCORE Spain: public perceptions of key government COVID-19 control measures. White TM, Cash-Gibson L, Martin-Moreno JM, Matesanz R, Crespo J, Alfonso-Sanchez JL, Villapol S, El-Mohandes A, Lazarus JV.Eur J Public Health. 2021 Oct 26;31(5):1095-1102. doi: 10.1093/eurpub/ckab066.PMID: 33872348 Free PMC article.

13.  More Than 50 Long-Term Effects of COVID-19: A Systematic Review and Meta-Analysis. Lopez-Leon S, Wegman-Ostrosky T, Perelman C, Sepulveda R, Rebolledo P, Cuapio A, Villapol S.Res Sq. 2021 Mar 1:rs.3.rs-266574. doi: 10.21203/rs.3.rs-266574/v1. Preprint.PMID: 33688642 Free PMC article. Updated.

14.  More than 50 Long-term effects of COVID-19: a systematic review and meta-analysis. Lopez-Leon S, Wegman-Ostrosky T, Perelman C, Sepulveda R, Rebolledo PA, Cuapio A, Villapol S.medRxiv. 2021 Jan 30:2021.01.27.21250617. doi: 10.1101/2021.01.27.21250617. Preprint.PMID: 33532785 Free PMC article. Updated.

15.  SARS-CoV-2 genomic diversity and the implications for qRT-PCR diagnostics and transmission. Sapoval N, Mahmoud M, Jochum MD, Liu Y, Elworth RAL, Wang Q, Albin D, Ogilvie HA, Lee MD, Villapol S, Hernandez KM, Maljkovic Berry I, Foox J, Beheshti A, Ternus K, Aagaard KM, Posada D, Mason CE, Sedlazeck FJ, Treangen TJ.Genome Res. 2021 Apr;31(4):635-644. doi: 10.1101/gr.268961.120. Epub 2021 Feb 18.PMID: 33602693 Free PMC article.

16.  Gastrointestinal symptoms associated with COVID-19: impact on the gut microbiome. Villapol S.Transl Res. 2020 Dec;226:57-69. doi: 10.1016/j.trsl.2020.08.004. Epub 2020 Aug 20.PMID: 32827705 Free PMC article. Review.

17.  Hidden genomic diversity of SARS-CoV-2: implications for qRT-PCR diagnostics and transmission. Sapoval N, Mahmoud M, Jochum MD, Liu Y, Elworth RAL, Wang Q, Albin D, Ogilvie H, Lee MD, Villapol S, Hernandez KM, Berry IM, Foox J, Beheshti A, Ternus K, Aagaard KM, Posada D, Mason CE, Sedlazeck F, Treangen TJ.bioRxiv. 2020 Jul 2:2020.07.02.184481. doi: 10.1101/2020.07.02.184481. Preprint.PMID: 32637955 Free PMC article. Updated.

18.  Serum Amyloid A is Expressed in the Brain After Traumatic Brain Injury in a Sex-Dependent Manner. Soriano S, Moffet B, Wicker E, Villapol S.Cell Mol Neurobiol. 2020 Oct;40(7):1199-1211. doi: 10.1007/s10571-020-00808-3. Epub 2020 Feb 14.PMID: 32060858 Free PMC article.

19.  Early Sex Differences in the Immune-Inflammatory Responses to Neonatal Ischemic Stroke. Villapol S, Faivre V, Joshi P, Moretti R, Besson VC, Charriaut-Marlangue C.Int J Mol Sci. 2019 Aug 4;20(15):3809. doi: 10.3390/ijms20153809.PMID: 31382688 Free PMC article.

20.  Serum Amyloid A Protein as a Potential Biomarker for Severity and Acute Outcome in Traumatic Brain Injury. Wicker E, Benton L, George K, Furlow W, Villapol S.Biomed Res Int. 2019 Apr 16;2019:5967816. doi: 10.1155/2019/5967816. eCollection 2019.PMID: 31119176 Free PMC article.

21.  Traumatic Brain Injury in Mice Induces Acute Bacterial Dysbiosis Within the Fecal Microbiome. Treangen TJ, Wagner J, Burns MP, Villapol S.Front Immunol. 2018 Nov 27;9:2757. doi: 10.3389/fimmu.2018.02757. eCollection 2018.PMID: 30546361 Free PMC article.

22.  Apolipoprotein E4 impairs spontaneous blood brain barrier repair following traumatic brain injury. Main BS, Villapol S, Sloley SS, Barton DJ, Parsadanian M, Agbaegbu C, Stefos K, McCann MS, Washington PM, Rodriguez OC, Burns MP.Mol Neurodegener. 2018 Apr 4;13(1):17. doi: 10.1186/s13024-018-0249-5.PMID: 29618365 Free PMC article. 

23.  Proteolytic Remodeling of Perineuronal Nets: Effects on Synaptic Plasticity and Neuronal Population Dynamics. Bozzelli PL, Alaiyed S, Kim E, Villapol S, Conant K.Neural Plast. 2018 Feb 4;2018:5735789. doi: 10.1155/2018/5735789. eCollection 2018.PMID: 29531525 Free PMC article. Review.

24.  Glial- and Neuronal-Specific Expression of CCL5 mRNA in the Rat Brain. Lanfranco MF, Mocchetti I, Burns MP, Villapol S.Front Neuroanat. 2018 Jan 12;11:137. doi: 10.3389/fnana.2017.00137. eCollection 2017.PMID: 29375328 Free PMC article.

25.  Combination of Fluorescent in situ Hybridization (FISH) and Immunofluorescence Imaging for Detection of Cytokine Expression in Microglia/Macrophage Cells. Fe Lanfranco M, Loane DJ, Mocchetti I, Burns MP, Villapol S.Bio Protoc. 2017 Nov 20;7(22):e2608. doi: 10.21769/BioProtoc.2608.PMID: 29238736 Free PMC article.

26.  Roles of Peroxisome Proliferator-Activated Receptor Gamma on Brain and Peripheral Inflammation. Villapol S.Cell Mol Neurobiol. 2018 Jan;38(1):121-132. doi: 10.1007/s10571-017-0554-5. Epub 2017 Oct 3.PMID: 28975471 Free PMC article. Review.

27.  Temporal Changes in Cortical and Hippocampal Expression of Genes Important for Brain Glucose Metabolism Following Controlled Cortical Impact Injury in Mice. Zhou J, Burns MP, Huynh L, Villapol S, Taub DD, Saavedra JM, Blackman MR.Front Endocrinol (Lausanne). 2017 Sep 11;8:231. doi: 10.3389/fendo.2017.00231. eCollection 2017.PMID: 28955302 Free PMC article.

28.  A Mouse Model of Single and Repetitive Mild Traumatic Brain Injury. Main BS, Sloley SS, Villapol S, Zapple DN, Burns MP.J Vis Exp. 2017 Jun 20;(124):55713. doi: 10.3791/55713.PMID: 28654066 Free PMC article.

29.  Sexual dimorphism in the inflammatory response to traumatic brain injury. Villapol S, Loane DJ, Burns MP.Glia. 2017 Sep;65(9):1423-1438. doi: 10.1002/glia.23171. Epub 2017 Jun 13.PMID: 28608978 Free PMC article.

30.  Reduced cortical excitatory synapse number in APOE4 mice is associated with increased calcineurin activity. Neustadtl AL, Winston CN, Parsadanian M, Main BS, Villapol S, Burns MP.Neuroreport. 2017 Jul 5;28(10):618-624. doi: 10.1097/WNR.0000000000000811.PMID: 28542068 Free PMC article.

31.  NOX2 deficiency alters macrophage phenotype through an IL-10/STAT3 dependent mechanism: implications for traumatic brain injury. Barrett JP, Henry RJ, Villapol S, Stoica BA, Kumar A, Burns MP, Faden AI, Loane DJ.J Neuroinflammation. 2017 Mar 24;14(1):65. doi: 10.1186/s12974-017-0843-4.PMID: 28340575 Free PMC article.

32.  Protease induced plasticity: matrix metalloproteinase-1 promotes neurostructural changes through activation of protease activated receptor 1. Allen M, Ghosh S, Ahern GP, Villapol S, Maguire-Zeiss KA, Conant K.Sci Rep. 2016 Oct 20;6:35497. doi: 10.1038/srep35497.PMID: 27762280 Free PMC article.

33.  Consequences of hepatic damage after traumatic brain injury: current outlook and potential therapeutic targets. Villapol S.Neural Regen Res. 2016 Feb;11(2):226-7. doi: 10.4103/1673-5374.177720.PMID: 27073366 Free PMC article. No abstract available.

34.  Dendritic Spine Loss and Chronic White Matter Inflammation in a Mouse Model of Highly Repetitive Head Trauma. Winston CN, Noël A, Neustadtl A, Parsadanian M, Barton DJ, Chellappa D, Wilkins TE, Alikhani AD, Zapple DN, Villapol S, Planel E, Burns MP.Am J Pathol. 2016 Mar;186(3):552-67. doi: 10.1016/j.ajpath.2015.11.006. Epub 2016 Feb 5.PMID: 26857506 Free PMC article.

35.  Deleting IGF-1 receptor from forebrain neurons confers neuroprotection during stroke and upregulates endocrine somatotropin. De Magalhaes Filho CD, Kappeler L, Dupont J, Solinc J, Villapol S, Denis C, Nosten-Bertrand M, Billard JM, Blaise A, Tronche F, Giros B, Charriaut-Marlangue C, Aïd S, Le Bouc Y, Holzenberger M.J Cereb Blood Flow Metab. 2017 Feb;37(2):396-412. doi: 10.1177/0271678X15626718. Epub 2016 Jul 20.PMID: 26762506 Free PMC article.

36.  Hepatic expression of serum amyloid A1 is induced by traumatic brain injury and modulated by telmisartan. Villapol S, Kryndushkin D, Balarezo MG, Campbell AM, Saavedra JM, Shewmaker FP, Symes AJ.Am J Pathol. 2015 Oct;185(10):2641-52. doi: 10.1016/j.ajpath.2015.06.016.PMID: 26435412 Free PMC article.

37.  Neurorestoration after traumatic brain injury through angiotensin II receptor blockage. Villapol S, Balarezo MG, Affram K, Saavedra JM, Symes AJ.Brain. 2015 Nov;138(Pt 11):3299-315. doi: 10.1093/brain/awv172. Epub 2015 Jun 26.PMID: 26115674 Free PMC article.

38.  Polypathology and dementia after brain trauma: Does brain injury trigger distinct neurodegenerative diseases, or should they be classified together as traumatic encephalopathy? Washington PM, Villapol S, Burns MP.Exp Neurol. 2016 Jan;275 Pt 3(0 3):381-388. doi: 10.1016/j.expneurol.2015.06.015. Epub 2015 Jun 16.PMID: 26091850 Free PMC article. Review.

39.  Neuroprotective effects of angiotensin receptor blockers. Villapol S, Saavedra JM.Am J Hypertens. 2015 Mar;28(3):289-99. doi: 10.1093/ajh/hpu197. Epub 2014 Oct 31.PMID: 25362113 Review.

40.  Temporal dynamics of cerebral blood flow, cortical damage, apoptosis, astrocyte-vasculature interaction and astrogliosis in the pericontusional region after traumatic brain injury. Villapol S, Byrnes KR, Symes AJ.Front Neurol. 2014 Jun 4;5:82. doi: 10.3389/fneur.2014.00082. eCollection 2014.PMID: 24926283 Free PMC article.

41.  Temporal patterns of cortical proliferation of glial cell populations after traumatic brain injury in mice. Susarla BT, Villapol S, Yi JH, Geller HM, Symes AJ.ASN Neuro. 2014 May 8;6(3):159-70. doi: 10.1042/AN20130034.PMID: 24670035 Free PMC article.

42.  Smad3 deficiency increases cortical and hippocampal neuronal loss following traumatic brain injury. Villapol S, Wang Y, Adams M, Symes AJ.Exp Neurol. 2013 Dec;250:353-65. doi: 10.1016/j.expneurol.2013.10.008. Epub 2013 Oct 9.PMID: 24120438

43.  Commercially available angiotensin II At₂ receptor antibodies are nonspecific. Hafko R, Villapol S, Nostramo R, Symes A, Sabban EL, Inagami T, Saavedra JM.PLoS One. 2013 Jul 1;8(7):e69234. doi: 10.1371/journal.pone.0069234. Print 2013.PMID: 23840911 Free PMC article.

44.  TGF-β superfamily gene expression and induction of the Runx1 transcription factor in adult neurogenic regions after brain injury. Logan TT, Villapol S, Symes AJ.PLoS One. 2013;8(3):e59250. doi: 10.1371/journal.pone.0059250. Epub 2013 Mar 21.PMID: 23555640 Free PMC article.

45.  Inhaled nitric oxide reduces brain damage by collateral recruitment in a neonatal stroke model. Charriaut-Marlangue C, Bonnin P, Gharib A, Leger PL, Villapol S, Pocard M, Gressens P, Renolleau S, Baud O.Stroke. 2012 Nov;43(11):3078-84. doi: 10.1161/STROKEAHA.112.664243. Epub 2012 Sep 4.PMID: 22949477

46.  Candesartan, an angiotensin II AT₁-receptor blocker and PPAR-γ agonist, reduces lesion volume and improves motor and memory function after traumatic brain injury in mice. Villapol S, Yaszemski AK, Logan TT, Sánchez-Lemus E, Saavedra JM, Symes AJ.Neuropsychopharmacology. 2012 Dec;37(13):2817-29. doi: 10.1038/npp.2012.152. Epub 2012 Aug 15.PMID: 22892395 Free PMC article.

47.  Dual action of NO synthases on blood flow and infarct volume consecutive to neonatal focal cerebral ischemia. Bonnin P, Leger PL, Villapol S, Deroide N, Gressens P, Pocard M, Renolleau S, Baud O, Charriaut-Marlangue C.Exp Neurol. 2012 Jul;236(1):50-7. doi: 10.1016/j.expneurol.2012.04.001. Epub 2012 Apr 12.PMID: 22531298

48.  Melatonin promotes myelination by decreasing white matter inflammation after neonatal stroke. Villapol S, Fau S, Renolleau S, Biran V, Charriaut-Marlangue C, Baud O.Pediatr Res. 2011 Jan;69(1):51-5. doi: 10.1203/PDR.0b013e3181fcb40b.PMID: 20856166

49.  Unilateral blood flow decrease induces bilateral and symmetric responses in the immature brain. Villapol S, Bonnin P, Fau S, Baud O, Renolleau S, Charriaut-Marlangue C.Am J Pathol. 2009 Nov;175(5):2111-20. doi: 10.2353/ajpath.2009.090257. Epub 2009 Oct 8.PMID: 19815715 Free PMC article.

50.  Astrocytic demise in the developing rat and human brain after hypoxic-ischemic damage. Gelot A, Villapol S, Billette de Villemeur T, Renolleau S, Charriaut-Marlangue C.Dev Neurosci. 2009;31(5):459-70. doi: 10.1159/000232564. Epub 2009 Aug 11.PMID: 19672074

51.  Astrocyte responses after neonatal ischemia: the yin and the yang. Villapol S, Gelot A, Renolleau S, Charriaut-Marlangue C.Neuroscientist. 2008 Aug;14(4):339-44. doi: 10.1177/1073858408316003. Epub 2008 Jul 8.PMID: 18612085 Review.

52.  Substantial migration of SVZ cells to the cortex results in the generation of new neurons in the excitotoxically damaged immature rat brain. Faiz M, Acarin L, Villapol S, Schulz S, Castellano B, Gonzalez B.Mol Cell Neurosci. 2008 Jun;38(2):170-82. doi: 10.1016/j.mcn.2008.02.002. Epub 2008 Mar 4.PMID: 18434192

53.  Survivin and heat shock protein 25/27 colocalize with cleaved caspase-3 in surviving reactive astrocytes following excitotoxicity to the immature brain. Villapol S, Acarin L, Faiz M, Castellano B, Gonzalez B.Neuroscience. 2008 Apr 22;153(1):108-19. doi: 10.1016/j.neuroscience.2008.01.054. Epub 2008 Feb 14.PMID: 18358624

54.  Distinct spatial and temporal activation of caspase pathways in neurons and glial cells after excitotoxic damage to the immature rat brain. Villapol S, Acarin L, Faiz M, Castellano B, Gonzalez B.J Neurosci Res. 2007 Dec;85(16):3545-56. doi: 10.1002/jnr.21450.PMID: 17668855

55.  Bilateral changes after neonatal ischemia in the P7 rat brain. Spiegler M, Villapol S, Biran V, Goyenvalle C, Mariani J, Renolleau S, Charriaut-Marlangue C.J Neuropathol Exp Neurol. 2007 Jun;66(6):481-90. doi: 10.1097/01.jnen.0000263875.22306.3c.PMID: 17549008

56.  Caspase-3 activation in astrocytes following postnatal excitotoxic damage correlates with cytoskeletal remodeling but not with cell death or proliferation. Acarin L, Villapol S, Faiz M, Rohn TT, Castellano B, González B.Glia. 2007 Jul;55(9):954-65. doi: 10.1002/glia.20518.PMID: 17487878 Free article.

57.  Antioxidant Cu/Zn SOD: expression in postnatal brain progenitor cells. Faiz M, Acarin L, Peluffo H, Villapol S, Castellano B, González B.Neurosci Lett. 2006 Jun 19;401(1-2):71-6. doi: 10.1016/j.neulet.2006.03.010. Epub 2006 Mar 29.PMID: 16567040