The Role of Gamma Delta T Cells in Autoimmune Rheumatic Diseases
Identifieur interne : 000936 ( Pmc/Curation ); précédent : 000935; suivant : 000937The Role of Gamma Delta T Cells in Autoimmune Rheumatic Diseases
Auteurs : Ilan BankSource :
- Cells [ 2073-4409 ] ; 2020.
Abstract
Autoimmune rheumatic diseases (ARDs), affecting ~1–1.5% of all humans, are associated with considerable life long morbidity and early mortality. Early studies in the 1990s showed numerical changes of the recently discovered γδ T cells in the peripheral blood and in affected tissues of patients with a variety of ARDs, kindling interest in their role in the immuno-pathogenesis of these chronic inflammatory conditions. Indeed, later studies applied rapid developments in the understanding of γδ T cell biology, including antigens recognized by γδ T cells, their developmental programs, states of activation, and cytokine production profiles, to analyze their contribution to the pathological immune response in these disorders. Here we review the published studies addressing the role of γδ T in the major autoimmune rheumatic diseases, including rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, systemic lupus erythematosus and scleroderma, and animal models thereof. Due to their unique properties spanning adaptive and innate immune functions, the ever deeper understanding of this unique T cell population is shedding new light on the pathogenesis of, while potentially enabling new therapeutic approaches to, these diseases.
Url:
DOI: 10.3390/cells9020462
PubMed: 32085540
PubMed Central: 7072729
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<front><div type="abstract" xml:lang="en"><p>Autoimmune rheumatic diseases (ARDs), affecting ~1–1.5% of all humans, are associated with considerable life long morbidity and early mortality. Early studies in the 1990s showed numerical changes of the recently discovered γδ T cells in the peripheral blood and in affected tissues of patients with a variety of ARDs, kindling interest in their role in the immuno-pathogenesis of these chronic inflammatory conditions. Indeed, later studies applied rapid developments in the understanding of γδ T cell biology, including antigens recognized by γδ T cells, their developmental programs, states of activation, and cytokine production profiles, to analyze their contribution to the pathological immune response in these disorders. Here we review the published studies addressing the role of γδ T in the major autoimmune rheumatic diseases, including rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, systemic lupus erythematosus and scleroderma, and animal models thereof. Due to their unique properties spanning adaptive and innate immune functions, the ever deeper understanding of this unique T cell population is shedding new light on the pathogenesis of, while potentially enabling new therapeutic approaches to, these diseases.</p>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Cells</journal-id>
<journal-id journal-id-type="iso-abbrev">Cells</journal-id>
<journal-id journal-id-type="publisher-id">cells</journal-id>
<journal-title-group><journal-title>Cells</journal-title>
</journal-title-group>
<issn pub-type="epub">2073-4409</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32085540</article-id>
<article-id pub-id-type="pmc">7072729</article-id>
<article-id pub-id-type="doi">10.3390/cells9020462</article-id>
<article-id pub-id-type="publisher-id">cells-09-00462</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>The Role of Gamma Delta T Cells in Autoimmune Rheumatic Diseases</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Bank</surname>
<given-names>Ilan</given-names>
</name>
</contrib>
</contrib-group>
<aff id="af1-cells-09-00462">Rheumatology Unit, Autoimmunity Center, Sheba Medical Center, Tel-Hashomer 52621, Israel;<email>ibank@tauex.tau.ac.il</email>
</aff>
<pub-date pub-type="epub"><day>18</day>
<month>2</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="collection"><month>2</month>
<year>2020</year>
</pub-date>
<volume>9</volume>
<issue>2</issue>
<elocation-id>462</elocation-id>
<history><date date-type="received"><day>15</day>
<month>1</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>15</day>
<month>2</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© 2020 by the author.</copyright-statement>
<copyright-year>2020</copyright-year>
<license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract><p>Autoimmune rheumatic diseases (ARDs), affecting ~1–1.5% of all humans, are associated with considerable life long morbidity and early mortality. Early studies in the 1990s showed numerical changes of the recently discovered γδ T cells in the peripheral blood and in affected tissues of patients with a variety of ARDs, kindling interest in their role in the immuno-pathogenesis of these chronic inflammatory conditions. Indeed, later studies applied rapid developments in the understanding of γδ T cell biology, including antigens recognized by γδ T cells, their developmental programs, states of activation, and cytokine production profiles, to analyze their contribution to the pathological immune response in these disorders. Here we review the published studies addressing the role of γδ T in the major autoimmune rheumatic diseases, including rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, systemic lupus erythematosus and scleroderma, and animal models thereof. Due to their unique properties spanning adaptive and innate immune functions, the ever deeper understanding of this unique T cell population is shedding new light on the pathogenesis of, while potentially enabling new therapeutic approaches to, these diseases.</p>
</abstract>
<kwd-group><kwd>gammadelta T cells</kwd>
<kwd>rheumatoid arthritis</kwd>
<kwd>systemic lupus erythematosus</kwd>
<kwd>systemic sclerosis</kwd>
<kwd>ankylosing spondylitis</kwd>
<kwd>juvenile idiopathic arthritis</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="cells-09-00462-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Participation of γδ T cells in Rheumatoid Arthritis. Vδ1<sup>+</sup>
γδ T cells using Vγ3, Vγ8 or other Vγ genes, recognize antigens presented by CD1d or MR1 on synovial fibroblasts, and/or antigens presented by antigen presenting cells, and secrete cytokines such as interleukin (IL)-17, IL-4, and IFNγ [<xref rid="B27-cells-09-00462" ref-type="bibr">27</xref>
,<xref rid="B37-cells-09-00462" ref-type="bibr">37</xref>
,<xref rid="B38-cells-09-00462" ref-type="bibr">38</xref>
,<xref rid="B40-cells-09-00462" ref-type="bibr">40</xref>
,<xref rid="B41-cells-09-00462" ref-type="bibr">41</xref>
,<xref rid="B48-cells-09-00462" ref-type="bibr">48</xref>
]. Chemokines produced in inflamed synovium, attract C-X-C motif chemokine receptor (CXCR)5 and C-C motif chemokine receptor (CCR)3 expressing Vγ9<sup>+</sup>
T cells to the synovium [<xref rid="B27-cells-09-00462" ref-type="bibr">27</xref>
]. These cells are activated by phosphoantigens presented by CD277 expressing cells in the synovium to express human leukocyte antigen (HLA)-DR, and in turn, may present antigens to CD4<sup>+</sup>
αβ T cells [<xref rid="B24-cells-09-00462" ref-type="bibr">24</xref>
]. Vδ1<sup>−</sup>
Vδ2<sup>−</sup>
γδ T cells recognizing unknown antigens also participate in the synovial reaction [<xref rid="B35-cells-09-00462" ref-type="bibr">35</xref>
]. IL-17 secreted by CD4<sup>+</sup>
αβ T cells activated by Vγ9<sup>+</sup>
γδ T cells may attract neutrophils and lead to osteoclastogenesis. In the presence of anti tumor necrosis factor (TNF)α antibodies, chemokines retaining the Vγ9<sup>+</sup>
T cells are decreased, and these cells migrate out of the joint to the peripheral blood. Peripheral blood γδ T cells express activation markers acquired in lymph nodes or as a reflection of activation in the synovium [<xref rid="B24-cells-09-00462" ref-type="bibr">24</xref>
,<xref rid="B25-cells-09-00462" ref-type="bibr">25</xref>
,<xref rid="B28-cells-09-00462" ref-type="bibr">28</xref>
].</p>
</caption>
<graphic xlink:href="cells-09-00462-g001"></graphic>
</fig>
<fig id="cells-09-00462-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Hypothetical model incorporating the immunopathogenetic role of γδ T cells in human systemic lupus erythematosus (SLE) and murine models. γδ T cells may become activated by plasmacytoid dendritic cells pDC in lymph nodes, leading to their secretion of proinflammatory cytokines such as IL-17 and IFNγ, an activity modulated by BLK [<xref rid="B93-cells-09-00462" ref-type="bibr">93</xref>
]. A subset of γδ T cells expressing CXCR5 release Wingless-related integration site (Wnt) proteins, that enhance differentiation of naïve T cells to become follicular helper T cells [<xref rid="B100-cells-09-00462" ref-type="bibr">100</xref>
], which in turn, together with IL-4 secretion [<xref rid="B97-cells-09-00462" ref-type="bibr">97</xref>
] differentiate B cells to become antigen producing cells making anti DNA antibodies. Other γδ T cells directly interact with heat shock protein (HSP)65 expressing B cells via their T cell receptor (TCR) and help drive anti DNA antibody secretion [<xref rid="B92-cells-09-00462" ref-type="bibr">92</xref>
]. At the same time regulatory FoxP3<sup>+</sup>
γδ T cells may become activated by transforming growth factor (TGF)β produced by pDC [<xref rid="B18-cells-09-00462" ref-type="bibr">18</xref>
], and by CD1d expressing cells in a TCR dependent manner, to downregulate the immune response [<xref rid="B99-cells-09-00462" ref-type="bibr">99</xref>
]. After activation in lymph nodes, γδ T cells could migrate to the kidney where they secrete IL-17, thus enhancing migration of leukocytes [<xref rid="B101-cells-09-00462" ref-type="bibr">101</xref>
].</p>
</caption>
<graphic xlink:href="cells-09-00462-g002"></graphic>
</fig>
<fig id="cells-09-00462-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Role of γδ T cells in human systemic sclerosis. On the right, representing patients without interstitial lung disease, are, cytotoxic granzyme expressing Vδ2<sup>+</sup>
γδ T cells in the peripheral blood, which are shown to interact with the endothelium via engagement of the TCR with CD277 endothelial molecules activated by isopentenyl pyrophosphate (IPP), while inducing the procoagulant tissue factor on monocytes, which together could lead to endothelial damage [<xref rid="B103-cells-09-00462" ref-type="bibr">103</xref>
,<xref rid="B107-cells-09-00462" ref-type="bibr">107</xref>
]. The peripheral blood is enriched in CD161<sup>+</sup>
Vδ1<sup>+</sup>
T cells [<xref rid="B104-cells-09-00462" ref-type="bibr">104</xref>
]. Profibrotic Vδ1<sup>+</sup>
cells may migrate to the lung, where they encounter cells expressing CD1d in complex with lipids, which trigger Vδ1<sup>+</sup>
T cells to secrete profibrotic factors (e.g., IL-4, CCL3) [<xref rid="B104-cells-09-00462" ref-type="bibr">104</xref>
,<xref rid="B105-cells-09-00462" ref-type="bibr">105</xref>
,<xref rid="B110-cells-09-00462" ref-type="bibr">110</xref>
]. Along with this, exit of Vδ2<sup>+</sup>
T cells (which may potentially confer anti fibrotic functions), from the lung to the peripheral blood takes place [<xref rid="B106-cells-09-00462" ref-type="bibr">106</xref>
,<xref rid="B111-cells-09-00462" ref-type="bibr">111</xref>
]. These alterations of γδ T cell composition in the lung may contribute to progressive lung disease.</p>
</caption>
<graphic xlink:href="cells-09-00462-g003"></graphic>
</fig>
<table-wrap id="cells-09-00462-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">cells-09-00462-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>Changes of γδ T cells in autoimmune rheumatic diseases.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Disease (Tissue)</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Total γδ T Cells (Relative to Normal)</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Vδ1<sup>+</sup>
T Cells (Relative to Normal)</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Vγ9Vδ2 T Cells (Relative to Normal)</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RA (PB)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Equal or decreased </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ratio relative to Vδ2 is increased. Sometimes includes oligoclonal expansions</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Equal or decreased (in established long term disease), increased VγδVδ2 TEMRA, decreased naïve Vγ9Vδ2 T cells. Sometimes include oligoclonal expansions. Increases noted after anti TNFα and gold salt therapy. Negative association with disease activity</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RA (synovium)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Polyclonal repertoire sometimes containing oligoclonal expansions common to different joints. HLADR expression increased, CD16 decreased.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Increased relative to Vδ2. Often using Vγ8 or Vγ3 along with Vδ1 in the TCR</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Relatively expanded compared to the PB, may use Jδ2.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B32-cells-09-00462" ref-type="bibr">32</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">JIA (PB)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">May be Increased in oligoarticular and quiescent systemic JIA otherwise equal. Increase of IL-17 producers in SJIA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Increase of Vδ1<sup>+</sup>
CD69<sup>+</sup>
T cells </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Increase of Vδ2<sup>+</sup>
CD69<sup>+</sup>
T cells</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B71-cells-09-00462" ref-type="bibr">71</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">JIA (synovium)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Higher than PB in oligoarticular JIA. Otherwise equal to percentage in PB</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Higher CD69<sup>+</sup>
than in PB, usually CD45RA<sup>+</sup>
, higher in ANA<sup>+</sup>
patients, inversely associated with age at onset, and with recurrence of synovitis</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Higher CD69<sup>+</sup>
than PB. Usually CD45RO<sup>+</sup>
<break></break>
inversely associated with age at onset, positively with recovery</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B74-cells-09-00462" ref-type="bibr">74</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AS (pB)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Total decreased, but enriched for IL23R<sup>+</sup>
γδ T cells secreting IL-17<break></break>
and in IL-17 and GM-CSF double producing γδ T cells</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Elevated in AS patients receiving anti TNFα, secrete IFNγ.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B80-cells-09-00462" ref-type="bibr">80</xref>
,<xref rid="B82-cells-09-00462" ref-type="bibr">82</xref>
,<xref rid="B83-cells-09-00462" ref-type="bibr">83</xref>
,<xref rid="B84-cells-09-00462" ref-type="bibr">84</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AS (enthesium/synovium) </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RORγt<sup>+</sup>
iNKT and γδ-hi T cells increased, producing IL-17</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Enriched for IL-23<sup>+</sup>
RORγt<sup>+</sup>
iNKT and γδ-hi</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B80-cells-09-00462" ref-type="bibr">80</xref>
,<xref rid="B82-cells-09-00462" ref-type="bibr">82</xref>
,<xref rid="B83-cells-09-00462" ref-type="bibr">83</xref>
,<xref rid="B84-cells-09-00462" ref-type="bibr">84</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SLE (pB)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Decreased, but increase of γδ T cells expressing CD69 and HLADR, and decrease of TNFα and IL-17 secreting cells. Inverse correlation with disease activity. γδ lines help anti DNA production by B cells</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">decreased, but increased in inactive SLE</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">decreased</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B18-cells-09-00462" ref-type="bibr">18</xref>
,<xref rid="B87-cells-09-00462" ref-type="bibr">87</xref>
,<xref rid="B88-cells-09-00462" ref-type="bibr">88</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SLE (skin)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">increased</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">increased</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B90-cells-09-00462" ref-type="bibr">90</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SSc [pB)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Decreased especially in early term disease (less than 3 years), diffuse disease and in SCL70<sup>+</sup>
patient. Otherwise equal.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Increased Vδ1<sup>+</sup>
and CD161<sup>+</sup>
Vδ1<sup>+</sup>
especially in patients without ILD. Increase of Vδ1<sup>+</sup>
CD49d<sup>+</sup>
, and HLADR<sup>+</sup>
cells. May be profibrotic in vitro, may respond to cardiolipin via CD1d</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Unchanged, decreased, or increased in some patients with ILD, increased granzyme expression, cytotoxic to endothelial cells. Induce fibroblast apoptosis. May be anti fibrotic.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B91-cells-09-00462" ref-type="bibr">91</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SSC (skin)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Increased, restricted clonality</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B88-cells-09-00462" ref-type="bibr">88</xref>
,<xref rid="B90-cells-09-00462" ref-type="bibr">90</xref>
,<xref rid="B92-cells-09-00462" ref-type="bibr">92</xref>
,<xref rid="B93-cells-09-00462" ref-type="bibr">93</xref>
,<xref rid="B94-cells-09-00462" ref-type="bibr">94</xref>
,<xref rid="B95-cells-09-00462" ref-type="bibr">95</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="cells-09-00462-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">cells-09-00462-t002_Table 2</object-id>
<label>Table 2</label>
<caption><p>γδ T cells in animal models of autoimmune rheumatic diseases.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Disease Model</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Role of γδ T Cells</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Rat adjuvant arthritis</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">No role in disease induction. Possible role in effector phase of disease.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B52-cells-09-00462" ref-type="bibr">52</xref>
,<xref rid="B53-cells-09-00462" ref-type="bibr">53</xref>
,<xref rid="B54-cells-09-00462" ref-type="bibr">54</xref>
,<xref rid="B55-cells-09-00462" ref-type="bibr">55</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Murine Collagen induced arthritis</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Vγ4/Vδ4<sup>+</sup>
cells producing IL-17 are pathogenic. IL-17 production can be suppressed by inhibitor of RORγt and by IL-28A. ES-62, a phosphorylcholine containing glycoprotein and IL-10 reduce migration of IL-17 producing γδ T cells to the inflamed joint, which are maintained by IL-23, and are not associated with bone destruction.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B58-cells-09-00462" ref-type="bibr">58</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Murine BSA induced arthritis</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">(RORγ)t<sup>+</sup>
IL-17 producing γδ T cells dependent upon IL-23 accumulated in arthritic joints.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B59-cells-09-00462" ref-type="bibr">59</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Murine non antigen dependent arthritis</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-1R and IL-23R expressing Vγ6<sup>+</sup>
γδ IL 17 cells are the main producers of IL-17 in joints of Il1rn <sup>-</sup>
/<sup>-</sup>
mice spontaneously developing arthritis. γδ T cells are responsible for arthritis in B10.RIII mice induced by gene transfer of IL-23. Arthritis induced by intraperitoneal injection of mannan is dependent upon IL-17 secreting γδ T cells.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B67-cells-09-00462" ref-type="bibr">67</xref>
,<xref rid="B68-cells-09-00462" ref-type="bibr">68</xref>
,<xref rid="B70-cells-09-00462" ref-type="bibr">70</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Murine IFNγ<sup>-</sup>
knockout (KO)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-17 secreting γδ T cells were shown to participate in arthritis and the systemic response to complete Freund adjuvant injection developing in these mice.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B79-cells-09-00462" ref-type="bibr">79</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Murine IL-23 gene introduction</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">increased number of γδ T cells are found in Achilles tendon enthesis, aortic root, and adjacent to the ciliary body and secreted IL-17.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B86-cells-09-00462" ref-type="bibr">86</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Murine MRL/lpr model of SLE</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">γδ T cells are protective from development of glomerulonephritis in the presence of αβ T cells, but mediate a less severe form of disease in their absence, mediated by cytokines and help for B cells. With age, some γδ T cells acquire a CD4<sup>+</sup>
B220<sup>+</sup>
phenotype, and produce IL-17. In BLK<sup>+/-</sup>
.lpr mice expressing low levels of Bruton lymphocyte kinase gene IL-17 and IFNγ producing γδ T cells are increased enhanced and mediate glomerular damage. γδ T cells induce phosphopeptide P140 mediated apoptosis of lymphocytes, which is associated with amelioration of disease in MRL/lpr mice.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B93-cells-09-00462" ref-type="bibr">93</xref>
,<xref rid="B94-cells-09-00462" ref-type="bibr">94</xref>
,<xref rid="B97-cells-09-00462" ref-type="bibr">97</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">lupus-prone NZB/NZW mice</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD1d restricted γδ T cells may be protective in young, and pathogenic in old mice.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B99-cells-09-00462" ref-type="bibr">99</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Pristane induced model of SLE</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">γδ T cells in the kidney expressed IL-17F and A and attracted neutrophils to the kidney. TCRδ<sup>-/-</sup>
mice developed milder glomerulonephritis, due to decreased T follicular helper cell differentiation dependent upon γδ T cell secretion of Wnt ligands.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B101-cells-09-00462" ref-type="bibr">101</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
</record>
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