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PORZIONATO, ANDREA (2009) Studio neuroanatomico dei centri di regolazione cardiorespiratoria: bulbo encefalico e glomo carotideo. [Ph.D. thesis]

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Abstract (english)

INTRODUCTION – Central and peripheral structures, as the medullary nuclei and the carotid body, strictly cohoperate for cardiovascular and respiratory regulation. In the literature, comprehensive and unbiased analyses of morphometric parameters and apoptosis phenomena in infant and adult medullary nuclei are still lacking. Data about local expression of different phosphodiesterase isoforms are also still poor. In the carotid body, many different neurotransmitters/neuromodulators, adhesion molecules and signalling transduction components have been identified but data are still lacking about the presence of some of these, such as adrenomedullin (AM), neurotensin receptors, Neural Cell Adhesion Molecule (NCAM), extracellular signal-regulated kinase (ERK), AKT. The aim of the present work was to give a comprehensive analysis of morphometric parameters and apoptosis phenomena in human medullary nuclei and to analyse the presence of the above components in the carotid body.
MATERIALS AND METHODS – Materials consisted of medullae oblongatae sampled at autopsy from 22 adults and 10 infants, and carotid bodies sampled at autopsy from 16 adult subjects and 6 foetuses. A morphometric analysis with the optical disector method was performed to calculate the neuronal densities, nuclear volumes and total neuron numbers of medullary nuclei. Apoptosis was also studied by terminal deoxynucleotidyl transferase-mediated dUTP nick end-labelling (TUNEL) and the mean percentages (± Standard Deviation) of TUNEL-positive neurons were morphometrically analysed. The regional distribution and cellular localization of four isozyme forms of the phosphodiesterase 4 (PDE4A, PDE4B, PDE4C and PDE4D) were also studied in 8 of the above adult subjects by in situ hybridization. In the study of the carotid body, we analysed by immunocytochemistry and double immunofluorescence the expression of AM, neurotensin receptor 1 (NTR1), NCAM, ERK and pERK, AKT and pAKT. AM, ERK/pERK and AKT/pAKT were also studied in foetal samples.
RESULTS – In both adults and infants, higher neuronal densities were found in the more ventrally located nuclei of the spinal trigeminal tract (NSTT) (mean values ± Standard Deviation: 9217±2146 n/mm3 and 21347±5006 n/mm3, respectively) and inferior olivary complex (PION: 9149±1341 n/mm3 and 20910±1582 n/mm3; MION: 10102±3024 n/mm3 and 19267±3475 n/mm3; DION: 11318±3704 n/mm3 and 23124±6740 n/mm3, respectively) than in the nuclei of the medullary tegmentum, i.e., hypoglossal nucleus (XII) (1070±343.4 n/mm3 and 2799±1292 n/mm3), dorsal motor nucleus of the vagus (DMNV) (1663±431.4 n/mm3 and 2915±568.1 n/mm3), nucleus tractus solitarii (NTS) (2982±639.9 n/mm3 and 8150±1735 n/mm3), medial vestibular nucleus (MedVe) (2964±380.8 n/mm3 and 6958±1076 n/mm3) and cuneate nucleus (Cu) (1061±238.7 n/mm3 and 2686±843.6 n/mm3). All the medullary nuclei showed higher volumes and lower neuronal densities in adults than in infants, without statistically significant differences in total neuron numbers. Statistically significant differences between adults and infants were found in the neuronal apoptotic indexes of the Cu (28.2±16.3% vs. 6.9±8.7%), MedVe (24.7±15.0% vs. 11.3±11.4%), NTS (11.2±11.2% vs. 2.3±2.4%), DMNV (6.8±8.5% vs. 0.1±0.2%) and XII (6.6±5.7% vs. 0.1±0.2%). Differences in neuronal apoptotic index were also statistically significant among nuclei, those with higher neuronal apoptotic indexes being the Cu, MedVe and NSTT. In the medullary nuclei PDE4B and PDE4D mRNA expression was abundant and distributed not only in neuronal cells, but also in glial cells, especially on and around blood vessels. The hybridization signals for PDE4B and PDE4D mRNAs in the AP were stronger than in any other nucleus considered. They were also found in vomiting-related nuclei such as NTS and DMNV. In the carotid body, no AM, NTR1, and NCAM immunoreactivities were visible in type II cells. Anti-NTR1 and -NCAM immunohistochemistries showed positivity in 45.6 ± 9.2% and 78.3 ± 7.2% of adult type I cells, respectively. Higher percentages of positive type I cells were found in adult than foetal subjects for anti-AM (32.3 ± 7.7% vs 11.8 ± 2.7%, P<0.001), -ERK (32.3 ± 7.7% vs 11.8 ± 2.7%, P<0.001), -pERK (32.3 ± 7.7% vs 11.8 ± 2.7%, P<0.001), -AKT (32.3 ± 7.7% vs 11.8 ± 2.7%, P<0.001) and -pAKT (32.3 ± 7.7% vs 11.8 ± 2.7%, P<0.001) immunohistochemistries.
DISCUSSION – The higher nuclear volumes and lower neuronal densities in adults may be ascribed to postnatal development of the neuropil and microvascularization. The higher apoptotic indexes in adults indicate higher resistance of infant neuronal populations to terminal hypoxic-ischaemic injury or post-mortem changes. Moreover, nuclei with higher apoptotic indexes are located in the lateral medullary tegmentum and share the same vascular supply from the posterior inferior cerebellar artery, suggesting different characteristics of survival on vascular basis. High PDE4 expression in the AP suggests that cAMP signaling modification could mediate the emetic effects of PDE4 inhibitors in human brainstem. Immunohistochemical findings in the carotid body suggest that AM and NT may play a role in the regulation of chemoreceptor discharge. The high expression level of NCAM in the carotid body indicates a role in regulating adhesion between type I cells. It may be hypothetized that the ERK and AKT signalling pathways in the carotid body are activated by neuromodulator/neurotrophic factors and plays a role in producing long-term cellular modifications. The lower expression of AM, ERK/pERK, and AKT/pAKT in foetuses may be ascribed to the absence of pulmonary respiration with lack of regulatory role of the carotid body during the prenatal period.

Abstract (italian)

INTRODUZIONE – Strutture nervose centrali e periferiche, quali i nuclei bulbari ed il glomo carotideo, cooperano alla regolazione cardiovascolare e respiratoria. Le conoscenze dei parametri morfometrici e dei fenomeni apoptotici nei nuclei bulbari di adulti e bambini, così come quelle relative all’espressione locale delle isoforme delle fosfodiesterasi, sono ancora limitate. Nel glomo carotideo sono stati individuati molti neurotrasmettitori/neuromodulatori differenti, molecole di adesione e componenti di vie di trasduzione del segnale ma non ci sono ancora dati sulla presenza di alcuni di essi, quali l’adrenomedullina (AM), i recettori della neurotensina, la molecola di adesione cellulare neurale (NCAM), la chinasi regolata da segnale extracellulare (ERK) ed AKT. Scopo del presente lavoro è fornire un’analisi completa dei parametri morfometrici e dei fenomeni apoptotici dei nuclei bulbari umani e analizzare la presenza delle componenti sovrariportate nel glomo carotideo.
MATERIALI E METODI – I materiali usati sono stati bulbi encefalici prelevati in corso di autopsia da 22 adulti e 10 bambini e glomi carotidei prelevati da 16 adulti e 6 feti. E’ stata effettuata un’analisi morfometrica con il metodo del dissettore ottico per calcolare le densità neuronali, i volumi nucleari e i numeri totali di neuroni dei nuclei bulbari. E’ stata altresì studiata l’apoptosi mediante terminal deoxynucleotidyl transferase-mediated dUTP nick end-labelling (TUNEL) e sono state analizzate morfometricamente le percentuali medie (± Deviazione Standard) dei neuroni TUNEL-positivi. E’ stata studiata la distribuzione regionale e cellulare delle quattro isoforme della fosfodiesterasi 4 (PDE4A, PDE4B, PDE4C e PDE4D) in 8 dei soggetti adulti mediante ibridazione in situ. Per quanto riguarda l’analisi dei glomi carotidei si è proceduto allo studio con immunoistochimica ed immunofluorescenza doppia dell’espressione di AM, recettore della neurotensina di tipo 1 (NTR1), NCAM, ERK e pERK, AKT e pAKT. L’analisi d’espressione di AM, ERK/pERK e AKT/pAKT è stata altresì effettuata su prelievi fetali.
RISULTATI – Sia negli adulti che nei bambini densità neuronali maggiori sono state trovate nei nuclei localizzati ventralmente, ossia il nucleo del tratto spinale del trigemino (NSTT) (valori medi ± Deviazione Standard: 9217±2146 n/mm3 e 21347±5006 n/mm3, rispettivamente) ed il complesso olivare inferiore (PION: 9149±1341 n/mm3 e 20910±1582 n/mm3; MION: 10102±3024 n/mm3 e 19267±3475 n/mm3; DION: 11318±3704 n/mm3 e 23124±6740 n/mm3, rispettivamente), che nei nuclei del tegmento bulbare, cioè il nucleo ipoglosso (XII) (1070±343,4 n/mm3 e 2799±1292 n/mm3), il nucleo motore dorsale del vago (DMNV) (1663±431,4 n/mm3 e 2915±568,1 n/mm3), il nucleo del tratto solitario (NTS) (2982±639,9 n/mm3 e 8150±1735 n/mm3), il nucleo vestibolare mediale (MedVe) (2964±380,8 n/mm3 e 6958±1076 n/mm3) ed il nucleo cuneato (Cu) (1061±238,7 n/mm3 e 2686±843,6 n/mm3). Tutti i nuclei bulbari presentavano volumi maggiori e densità neuronali minori negli adulti rispetto ai bambini, senza differenze statisticamente significative nel numero totale di neuroni. Differenze statisticamente significative tra adulti e bambini sono state trovate negli indici apoptotici neuronali del Cu (28,2±16,3% vs. 6,9±8,7%), MedVe (24,7±15,0% vs. 11,3±11,4%), NTS (11,2±11,2% vs. 2,3±2,4%), DMNV (6,8±8,5% vs. 0,1±0,2%) e XII (6,6±5,7% vs. 0,1±0,2%). Differenze statisticamente significative erano altresì presenti per quanto riguarda il confronto tra i diversi nuclei, con il Cu, il MedVe ed il NSTT che mostravano i maggiori indici apoptotici neuronali. Nei nuclei bulbari l’mRNA di PDE4B e PDE4D era abbondante e distribuito non solo nelle cellule neuronali ma anche nelle cellule gliali, soprattutto in vicinanza dei vasi sanguigni. I segnali di ibridazione per PDE4B e PDE4D erano più intensi nell’AP che in ogni altro nucleo considerato. Sono stati altresì trovati in nuclei implicati nei meccanismi del vomito come il NTS ed il DMNV. Nel glomo carotideo non sono state rilevate immunoreattività per AM, NTR1, e NCAM a carico delle cellule di tipo II di entrambe le casistiche. Analisi immunoistochimiche anti-NTR1 ed –NCAM hanno evidenziato positività del 45,6±9,2% e 78,3±7,2% delle cellule di I tipo dei soggetti adulti, rispettivamente. Percentuali maggiori di cellule di tipo I positive sono state trovate negli adulti rispetto ai feti all’esame immunoistochimico per AM (32,3±7,7% vs 11,8±2,7%, P<0,001), ERK (32,3±7,7% vs 11,8±2,7%, P<0,001), pErk (32,3±7,7% vs 11,8±2,7%, P<0,001), Akt (32,3±7,7% vs 11,8±2,7%, P<0,001) e pAkt (32,3±7,7% vs 11,8±2,7%, P<0,001).
DISCUSSIONE – I maggiori volumi nucleari e le minori densità neuronali rilevati negli adulti possono essere ascritti allo sviluppo postnatale del neuropilo e delle microvascolarizzazione. I maggiori indici apoptotici neuronali rilevati negli adulti indicano una maggiore resistenza delle popolazioni neuronali infantili agli insulti ipossico-ischemici o ai cambiamenti postmortali. Inoltre i nuclei con maggiori indici apoptotici sono localizzati nel tegmento bulbare laterale e condividono la stessa irrorazione vascolare dall’arteria cerebellare posteriore inferiore, suggerendo differenti caratteristiche di sopravvivenza su base vascolare. L’elevata espressione di PDE4 nell’AP suggerisce che modificazioni delle vie del segnale che coinvolgono cAMP possano mediare gli effetti emetici degli inibitori di PDE4 nei tronchi encefalici umani. I reperti immunoistochimici nel glomo carotideo suggeriscono che l’AM e la NT possano svolgere un ruolo nella regolazione dell’attività chemorecettoriale del glomo. L’elevato livello di espressione di NCAM nel glomo carotideo indica un ruolo nella regolazione dell’adesione tra cellule di tipo I. Si può altresì ipotizzare l’attivazione delle vie di trasduzione del segnale ERK e AKT da parte di neuromodulatori/fattori neurotrofici, con possibile ruolo nella produzione di modificazioni cellulari a lungo termine. La minore espressione di AM, ERK/pERK, ed AKT/pAKT nei feti può essere ricondotta all’assenza di respirazione polmonare con mancanza del ruolo regolatorio del glomo carotideo durante il periodo prenatale.

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EPrint type:Ph.D. thesis
Ph.D. course:Ciclo 21 > Scuole per il 21simo ciclo > SCIENZE MEDICHE, CLINICHE E SPERIMENTALI > NEUROSCIENZE
Data di deposito della tesi:29 January 2009
Anno di Pubblicazione:2009
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/16 Anatomia umana
Struttura di riferimento:Dipartimenti > pre 2012 - Dipartimento di Anatomia e Fisiologia Umana
Codice ID:1604
Depositato il:29 Jan 2009
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