Nitric oxide synthase and neuronal vulnerability in parkinson's disease
Identifieur interne : 001F07 ( Istex/Corpus ); précédent : 001F06; suivant : 001F08Nitric oxide synthase and neuronal vulnerability in parkinson's disease
Auteurs : S. Hunot ; F. Boissière ; B. Faucheux ; B. Brugg ; A. Mouatt-Prigent ; Y. Agid ; E. C. HirschSource :
- Neuroscience [ 0306-4522 ] ; 1996.
English descriptors
- KwdEn :
Abstract
Abstract: Parkinson's disease is characterized by a loss of dopaminergic neurons in the mesencephalon. Although the mechanism of this neuronal loss is still unknown, oxidative stress is very likely involved in the cascade of events leading to nerve cell death. Since nitric oxide could be involved in the production of free radicals, we analysed, using immunohistochemistry and histochemistry, the production systems of nitric oxide in the mesencephalon of four patients with idiopathic Parkinson's disease and three matched control subjects. Using specific antibodies directed against the inducible isoform of nitric oxide synthase (the enzyme involved in the synthesis of nitric oxide), we found evidence to suggest that this isoform was present solely in glial cells displaying the morphological characteristics of activated macrophages. Immunohistochemical analysis performed with antibodies against the neuronal isoform of nitric oxide synthase, however, revealed perikarya and processes of neurons but no glial cell staining. The number of nitric oxide synthase-containing cells was investigated by histoenzymology, using the NADPH-diaphorase activity of nitric oxide synthase. Histochemistry revealed (i) a significant increase in NADPH-diaphorasepositive glial cell density in the dopaminergic cell groups characterized by neuronal loss in Parkinson's disease and (ii) a neuronal loss in Parkinson's disease that was two-fold greater for pigmented NADPH-diaphorase-negative neurons than for pigmented NADPH-diaphorase-positive neurons.These data suggest a potentially deleterious role of glial cells producing excessive levels of nitric oxide in Parkinson's disease, which may be neurotoxic for a subpopulation of dopaminergic neurons, especially those not expressing NADPH-diaphorase activity. However, it cannot be excluded that the presence of glial cells expressing nitric oxide synthase in the substantia nigra of patients with Parkinson's disease represents a consequence of dopaminergic neuronal loss.
Url:
DOI: 10.1016/0306-4522(95)00578-1
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<front><div type="abstract" xml:lang="en">Abstract: Parkinson's disease is characterized by a loss of dopaminergic neurons in the mesencephalon. Although the mechanism of this neuronal loss is still unknown, oxidative stress is very likely involved in the cascade of events leading to nerve cell death. Since nitric oxide could be involved in the production of free radicals, we analysed, using immunohistochemistry and histochemistry, the production systems of nitric oxide in the mesencephalon of four patients with idiopathic Parkinson's disease and three matched control subjects. Using specific antibodies directed against the inducible isoform of nitric oxide synthase (the enzyme involved in the synthesis of nitric oxide), we found evidence to suggest that this isoform was present solely in glial cells displaying the morphological characteristics of activated macrophages. Immunohistochemical analysis performed with antibodies against the neuronal isoform of nitric oxide synthase, however, revealed perikarya and processes of neurons but no glial cell staining. The number of nitric oxide synthase-containing cells was investigated by histoenzymology, using the NADPH-diaphorase activity of nitric oxide synthase. Histochemistry revealed (i) a significant increase in NADPH-diaphorasepositive glial cell density in the dopaminergic cell groups characterized by neuronal loss in Parkinson's disease and (ii) a neuronal loss in Parkinson's disease that was two-fold greater for pigmented NADPH-diaphorase-negative neurons than for pigmented NADPH-diaphorase-positive neurons.These data suggest a potentially deleterious role of glial cells producing excessive levels of nitric oxide in Parkinson's disease, which may be neurotoxic for a subpopulation of dopaminergic neurons, especially those not expressing NADPH-diaphorase activity. However, it cannot be excluded that the presence of glial cells expressing nitric oxide synthase in the substantia nigra of patients with Parkinson's disease represents a consequence of dopaminergic neuronal loss.</div>
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<abstract>Abstract: Parkinson's disease is characterized by a loss of dopaminergic neurons in the mesencephalon. Although the mechanism of this neuronal loss is still unknown, oxidative stress is very likely involved in the cascade of events leading to nerve cell death. Since nitric oxide could be involved in the production of free radicals, we analysed, using immunohistochemistry and histochemistry, the production systems of nitric oxide in the mesencephalon of four patients with idiopathic Parkinson's disease and three matched control subjects. Using specific antibodies directed against the inducible isoform of nitric oxide synthase (the enzyme involved in the synthesis of nitric oxide), we found evidence to suggest that this isoform was present solely in glial cells displaying the morphological characteristics of activated macrophages. Immunohistochemical analysis performed with antibodies against the neuronal isoform of nitric oxide synthase, however, revealed perikarya and processes of neurons but no glial cell staining. The number of nitric oxide synthase-containing cells was investigated by histoenzymology, using the NADPH-diaphorase activity of nitric oxide synthase. Histochemistry revealed (i) a significant increase in NADPH-diaphorasepositive glial cell density in the dopaminergic cell groups characterized by neuronal loss in Parkinson's disease and (ii) a neuronal loss in Parkinson's disease that was two-fold greater for pigmented NADPH-diaphorase-negative neurons than for pigmented NADPH-diaphorase-positive neurons.These data suggest a potentially deleterious role of glial cells producing excessive levels of nitric oxide in Parkinson's disease, which may be neurotoxic for a subpopulation of dopaminergic neurons, especially those not expressing NADPH-diaphorase activity. However, it cannot be excluded that the presence of glial cells expressing nitric oxide synthase in the substantia nigra of patients with Parkinson's disease represents a consequence of dopaminergic neuronal loss.</abstract>
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<author xml:id="author-1"><persName><forename type="first">S.</forename>
<surname>Hunot</surname>
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<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
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<author xml:id="author-2"><persName><forename type="first">F.</forename>
<surname>Boissière</surname>
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<author xml:id="author-3"><persName><forename type="first">B.</forename>
<surname>Faucheux</surname>
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<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
</author>
<author xml:id="author-4"><persName><forename type="first">B.</forename>
<surname>Brugg</surname>
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<author xml:id="author-5"><persName><forename type="first">A.</forename>
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<author xml:id="author-6"><persName><forename type="first">Y.</forename>
<surname>Agid</surname>
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<author xml:id="author-7"><persName><forename type="first">E.C.</forename>
<surname>Hirsch</surname>
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<affiliation>To whom correspondence should be addressed.</affiliation>
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<abstract xml:lang="en"><p>Abstract: Parkinson's disease is characterized by a loss of dopaminergic neurons in the mesencephalon. Although the mechanism of this neuronal loss is still unknown, oxidative stress is very likely involved in the cascade of events leading to nerve cell death. Since nitric oxide could be involved in the production of free radicals, we analysed, using immunohistochemistry and histochemistry, the production systems of nitric oxide in the mesencephalon of four patients with idiopathic Parkinson's disease and three matched control subjects. Using specific antibodies directed against the inducible isoform of nitric oxide synthase (the enzyme involved in the synthesis of nitric oxide), we found evidence to suggest that this isoform was present solely in glial cells displaying the morphological characteristics of activated macrophages. Immunohistochemical analysis performed with antibodies against the neuronal isoform of nitric oxide synthase, however, revealed perikarya and processes of neurons but no glial cell staining. The number of nitric oxide synthase-containing cells was investigated by histoenzymology, using the NADPH-diaphorase activity of nitric oxide synthase. Histochemistry revealed (i) a significant increase in NADPH-diaphorasepositive glial cell density in the dopaminergic cell groups characterized by neuronal loss in Parkinson's disease and (ii) a neuronal loss in Parkinson's disease that was two-fold greater for pigmented NADPH-diaphorase-negative neurons than for pigmented NADPH-diaphorase-positive neurons.These data suggest a potentially deleterious role of glial cells producing excessive levels of nitric oxide in Parkinson's disease, which may be neurotoxic for a subpopulation of dopaminergic neurons, especially those not expressing NADPH-diaphorase activity. However, it cannot be excluded that the presence of glial cells expressing nitric oxide synthase in the substantia nigra of patients with Parkinson's disease represents a consequence of dopaminergic neuronal loss.</p>
</abstract>
<textClass xml:lang="en"><keywords scheme="keyword"><list><head>Keywords</head>
<item><term>dopamine</term>
</item>
<item><term>human</term>
</item>
<item><term>NADPH-diaphorase</term>
</item>
<item><term>neurodegeneration</term>
</item>
<item><term>nitric oxide</term>
</item>
<item><term>mesencephalon</term>
</item>
</list>
</keywords>
</textClass>
<textClass xml:lang="en"><keywords scheme="keyword"><list><head>Abbreviations</head>
<item><term>A8</term>
<term>catecholaminergic cell group A8</term>
</item>
<item><term>eNOS</term>
<term>endothelial nitric oxide synthase</term>
</item>
<item><term>IFNγ</term>
<term>interferongamma</term>
</item>
<item><term>ILI-β</term>
<term>interleukin 1-beta</term>
</item>
<item><term>iNOS</term>
<term>inducible nitric oxide synthase</term>
</item>
<item><term>NADPH</term>
<term>nicotinamide adenine dinucleotide phosphate</term>
</item>
<item><term>NGS</term>
<term>normal goat serum</term>
</item>
<item><term>nNOS</term>
<term>neuronal nitric oxide synthase</term>
</item>
<item><term>NO</term>
<term>nitric oxide</term>
</item>
<item><term>NOS</term>
<term>nitric oxide synthase</term>
</item>
<item><term>O2−</term>
<term>superoxide radical</term>
</item>
<item><term>ONOO−</term>
<term>peroxynitrite</term>
</item>
<item><term>PBS</term>
<term>phosphate-buffered saline</term>
</item>
<item><term>PD</term>
<term>Parkinson's disease</term>
</item>
<item><term>SN</term>
<term>substantia nigra</term>
</item>
<item><term>SNpc</term>
<term>substantia nigra pars compacta</term>
</item>
<item><term>TBS</term>
<term>Tris-buffered saline</term>
</item>
<item><term>TNF-α</term>
<term>tumor necrosis factor-alpha</term>
</item>
<item><term>VTA</term>
<term>ventral tegmental area</term>
</item>
</list>
</keywords>
</textClass>
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<head><ce:title>Nitric oxide synthase and neuronal vulnerability in parkinson's disease</ce:title>
<ce:author-group><ce:author><ce:given-name>S.</ce:given-name>
<ce:surname>Hunot</ce:surname>
</ce:author>
<ce:author><ce:given-name>F.</ce:given-name>
<ce:surname>Boissière</ce:surname>
</ce:author>
<ce:author><ce:given-name>B.</ce:given-name>
<ce:surname>Faucheux</ce:surname>
</ce:author>
<ce:author><ce:given-name>B.</ce:given-name>
<ce:surname>Brugg</ce:surname>
</ce:author>
<ce:author><ce:given-name>A.</ce:given-name>
<ce:surname>Mouatt-Prigent</ce:surname>
</ce:author>
<ce:author><ce:given-name>Y.</ce:given-name>
<ce:surname>Agid</ce:surname>
</ce:author>
<ce:author><ce:given-name>E.C.</ce:given-name>
<ce:surname>Hirsch</ce:surname>
<ce:cross-ref refid="cor1"><ce:sup>*</ce:sup>
</ce:cross-ref>
</ce:author>
<ce:affiliation><ce:textfn>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</ce:textfn>
</ce:affiliation>
<ce:correspondence id="cor1"><ce:label>*</ce:label>
<ce:text>To whom correspondence should be addressed.</ce:text>
</ce:correspondence>
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<ce:date-accepted day="4" month="12" year="1995"></ce:date-accepted>
<ce:abstract id="ab1" class="author" xml:lang="en"><ce:section-title>Abstract</ce:section-title>
<ce:abstract-sec><ce:simple-para>Parkinson's disease is characterized by a loss of dopaminergic neurons in the mesencephalon. Although the mechanism of this neuronal loss is still unknown, oxidative stress is very likely involved in the cascade of events leading to nerve cell death. Since nitric oxide could be involved in the production of free radicals, we analysed, using immunohistochemistry and histochemistry, the production systems of nitric oxide in the mesencephalon of four patients with idiopathic Parkinson's disease and three matched control subjects. Using specific antibodies directed against the inducible isoform of nitric oxide synthase (the enzyme involved in the synthesis of nitric oxide), we found evidence to suggest that this isoform was present solely in glial cells displaying the morphological characteristics of activated macrophages. Immunohistochemical analysis performed with antibodies against the neuronal isoform of nitric oxide synthase, however, revealed perikarya and processes of neurons but no glial cell staining. The number of nitric oxide synthase-containing cells was investigated by histoenzymology, using the NADPH-diaphorase activity of nitric oxide synthase. Histochemistry revealed (i) a significant increase in NADPH-diaphorasepositive glial cell density in the dopaminergic cell groups characterized by neuronal loss in Parkinson's disease and (ii) a neuronal loss in Parkinson's disease that was two-fold greater for pigmented NADPH-diaphorase-negative neurons than for pigmented NADPH-diaphorase-positive neurons.</ce:simple-para>
<ce:simple-para>These data suggest a potentially deleterious role of glial cells producing excessive levels of nitric oxide in Parkinson's disease, which may be neurotoxic for a subpopulation of dopaminergic neurons, especially those not expressing NADPH-diaphorase activity. However, it cannot be excluded that the presence of glial cells expressing nitric oxide synthase in the substantia nigra of patients with Parkinson's disease represents a consequence of dopaminergic neuronal loss.</ce:simple-para>
</ce:abstract-sec>
</ce:abstract>
<ce:keywords class="keyword"><ce:section-title>Keywords</ce:section-title>
<ce:keyword><ce:text>dopamine</ce:text>
</ce:keyword>
<ce:keyword><ce:text>human</ce:text>
</ce:keyword>
<ce:keyword><ce:text>NADPH-diaphorase</ce:text>
</ce:keyword>
<ce:keyword><ce:text>neurodegeneration</ce:text>
</ce:keyword>
<ce:keyword><ce:text>nitric oxide</ce:text>
</ce:keyword>
<ce:keyword><ce:text>mesencephalon</ce:text>
</ce:keyword>
</ce:keywords>
<ce:keywords class="abr"><ce:section-title>Abbreviations</ce:section-title>
<ce:keyword><ce:text>A8</ce:text>
<ce:keyword><ce:text>catecholaminergic cell group A8</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>eNOS</ce:text>
<ce:keyword><ce:text>endothelial nitric oxide synthase</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>IFNγ</ce:text>
<ce:keyword><ce:text>interferongamma</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>ILI-β</ce:text>
<ce:keyword><ce:text>interleukin 1-beta</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>iNOS</ce:text>
<ce:keyword><ce:text>inducible nitric oxide synthase</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>NADPH</ce:text>
<ce:keyword><ce:text>nicotinamide adenine dinucleotide phosphate</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>NGS</ce:text>
<ce:keyword><ce:text>normal goat serum</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>nNOS</ce:text>
<ce:keyword><ce:text>neuronal nitric oxide synthase</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>NO</ce:text>
<ce:keyword><ce:text>nitric oxide</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>NOS</ce:text>
<ce:keyword><ce:text>nitric oxide synthase</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>O<ce:inf>2</ce:inf>
<ce:sup>−</ce:sup>
</ce:text>
<ce:keyword><ce:text>superoxide radical</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>ONOO<ce:sup>−</ce:sup>
</ce:text>
<ce:keyword><ce:text>peroxynitrite</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>PBS</ce:text>
<ce:keyword><ce:text>phosphate-buffered saline</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>PD</ce:text>
<ce:keyword><ce:text>Parkinson's disease</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>SN</ce:text>
<ce:keyword><ce:text>substantia nigra</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>SNpc</ce:text>
<ce:keyword><ce:text>substantia nigra pars compacta</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>TBS</ce:text>
<ce:keyword><ce:text>Tris-buffered saline</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>TNF-α</ce:text>
<ce:keyword><ce:text>tumor necrosis factor-alpha</ce:text>
</ce:keyword>
</ce:keyword>
<ce:keyword><ce:text>VTA</ce:text>
<ce:keyword><ce:text>ventral tegmental area</ce:text>
</ce:keyword>
</ce:keyword>
</ce:keywords>
</head>
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<mods version="3.6"><titleInfo lang="en"><title>Nitric oxide synthase and neuronal vulnerability in parkinson's disease</title>
</titleInfo>
<titleInfo type="alternative" lang="en" contentType="CDATA"><title>Nitric oxide synthase and neuronal vulnerability in parkinson's disease</title>
</titleInfo>
<name type="personal"><namePart type="given">S.</namePart>
<namePart type="family">Hunot</namePart>
<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
<role><roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal"><namePart type="given">F.</namePart>
<namePart type="family">Boissière</namePart>
<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
<role><roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal"><namePart type="given">B.</namePart>
<namePart type="family">Faucheux</namePart>
<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
<role><roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal"><namePart type="given">B.</namePart>
<namePart type="family">Brugg</namePart>
<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
<role><roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal"><namePart type="given">A.</namePart>
<namePart type="family">Mouatt-Prigent</namePart>
<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
<role><roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal"><namePart type="given">Y.</namePart>
<namePart type="family">Agid</namePart>
<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
<role><roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal"><namePart type="given">E.C.</namePart>
<namePart type="family">Hirsch</namePart>
<affiliation>INSERM U289, Physiopathologie et Pathogenèse des Maladies Dégénératives du Système Nerveux, Hoˆpital de la Salpêtrière, 47 bd de l'Hoˆpital, 75013 Paris, France</affiliation>
<description>To whom correspondence should be addressed.</description>
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<copyrightDate encoding="w3cdtf">1996</copyrightDate>
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<abstract lang="en">Abstract: Parkinson's disease is characterized by a loss of dopaminergic neurons in the mesencephalon. Although the mechanism of this neuronal loss is still unknown, oxidative stress is very likely involved in the cascade of events leading to nerve cell death. Since nitric oxide could be involved in the production of free radicals, we analysed, using immunohistochemistry and histochemistry, the production systems of nitric oxide in the mesencephalon of four patients with idiopathic Parkinson's disease and three matched control subjects. Using specific antibodies directed against the inducible isoform of nitric oxide synthase (the enzyme involved in the synthesis of nitric oxide), we found evidence to suggest that this isoform was present solely in glial cells displaying the morphological characteristics of activated macrophages. Immunohistochemical analysis performed with antibodies against the neuronal isoform of nitric oxide synthase, however, revealed perikarya and processes of neurons but no glial cell staining. The number of nitric oxide synthase-containing cells was investigated by histoenzymology, using the NADPH-diaphorase activity of nitric oxide synthase. Histochemistry revealed (i) a significant increase in NADPH-diaphorasepositive glial cell density in the dopaminergic cell groups characterized by neuronal loss in Parkinson's disease and (ii) a neuronal loss in Parkinson's disease that was two-fold greater for pigmented NADPH-diaphorase-negative neurons than for pigmented NADPH-diaphorase-positive neurons.These data suggest a potentially deleterious role of glial cells producing excessive levels of nitric oxide in Parkinson's disease, which may be neurotoxic for a subpopulation of dopaminergic neurons, especially those not expressing NADPH-diaphorase activity. However, it cannot be excluded that the presence of glial cells expressing nitric oxide synthase in the substantia nigra of patients with Parkinson's disease represents a consequence of dopaminergic neuronal loss.</abstract>
<subject lang="en"><genre>Keywords</genre>
<topic>dopamine</topic>
<topic>human</topic>
<topic>NADPH-diaphorase</topic>
<topic>neurodegeneration</topic>
<topic>nitric oxide</topic>
<topic>mesencephalon</topic>
</subject>
<subject lang="en"><genre>Abbreviations</genre>
<topic>A8 : catecholaminergic cell group A8</topic>
<topic>eNOS : endothelial nitric oxide synthase</topic>
<topic>IFNγ : interferongamma</topic>
<topic>ILI-β : interleukin 1-beta</topic>
<topic>iNOS : inducible nitric oxide synthase</topic>
<topic>NADPH : nicotinamide adenine dinucleotide phosphate</topic>
<topic>NGS : normal goat serum</topic>
<topic>nNOS : neuronal nitric oxide synthase</topic>
<topic>NO : nitric oxide</topic>
<topic>NOS : nitric oxide synthase</topic>
<topic>O2− : superoxide radical</topic>
<topic>ONOO− : peroxynitrite</topic>
<topic>PBS : phosphate-buffered saline</topic>
<topic>PD : Parkinson's disease</topic>
<topic>SN : substantia nigra</topic>
<topic>SNpc : substantia nigra pars compacta</topic>
<topic>TBS : Tris-buffered saline</topic>
<topic>TNF-α : tumor necrosis factor-alpha</topic>
<topic>VTA : ventral tegmental area</topic>
</subject>
<relatedItem type="host"><titleInfo><title>Neuroscience</title>
</titleInfo>
<titleInfo type="abbreviated"><title>NSC</title>
</titleInfo>
<genre type="journal">journal</genre>
<originInfo><dateIssued encoding="w3cdtf">199605</dateIssued>
</originInfo>
<identifier type="ISSN">0306-4522</identifier>
<identifier type="PII">S0306-4522(00)X0007-3</identifier>
<part><date>199605</date>
<detail type="volume"><number>72</number>
<caption>vol.</caption>
</detail>
<detail type="issue"><number>2</number>
<caption>no.</caption>
</detail>
<extent unit="issue pages"><start>309</start>
<end>592</end>
</extent>
<extent unit="pages"><start>355</start>
<end>363</end>
</extent>
</part>
</relatedItem>
<identifier type="istex">B157D8785BAACB7BB3EC52E539A7FBA2A93B5D7C</identifier>
<identifier type="DOI">10.1016/0306-4522(95)00578-1</identifier>
<identifier type="PII">0306-4522(95)00578-1</identifier>
<identifier type="ArticleID">95005781</identifier>
<accessCondition type="use and reproduction" contentType="copyright">©1996 IBRO</accessCondition>
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