An IL-17–dominant immune profile is shared across the major orphan forms of ichthyosis
The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood. We sought to characterize molecularly cutaneous inflammation and its c...
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| Published in | Journal of allergy and clinical immunology Vol. 139; no. 1; pp. 152 - 165 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.01.2017
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood.
We sought to characterize molecularly cutaneous inflammation and its correlation with clinical and barrier characteristics.
We analyzed biopsy specimens from 21 genotyped patients with ichthyosis (congenital ichthyosiform erythroderma, n = 6; lamellar ichthyosis, n = 7; epidermolytic ichthyosis, n = 5; and Netherton syndrome, n = 3) using immunohistochemistry and RT-PCR and compared them with specimens from healthy control subjects, patients with atopic dermatitis (AD), and patients with psoriasis. Clinical measures included the Ichthyosis Area Severity Index (IASI), which integrates erythema (IASI-E) and scaling (IASI-S); transepidermal water loss; and pruritus.
Ichthyosis samples showed increased epidermal hyperplasia (increased thickness and keratin 16 expression) and T-cell and dendritic cell infiltrates. Increases of general inflammatory (IL-2), innate (IL-1β), and some TH1/interferon (IFN-γ) markers in patients with ichthyosis were comparable with those in patients with psoriasis or AD. TNF-α levels in patients with ichthyosis were increased only in those with Netherton syndrome but were much lower than in patients with psoriasis and those with AD. Expression of TH2 cytokines (IL-13 and IL-31) was similar to that seen in control subjects. The striking induction of IL-17–related genes or markers synergistically induced by IL-17 and TNF-α (IL-17A/C, IL-19, CXCL1, PI3, CCL20, and IL36G; P < .05) in patients with ichthyosis was similar to that seen in patients with psoriasis. IASI and IASI-E scores strongly correlated with IL-17A (r = 0.74, P < .001) and IL-17/TNF–synergistic/additive gene expression. These markers also significantly correlated with transepidermal water loss, suggesting a link between the barrier defect and inflammation in patients with ichthyosis.
Our data associate a shared TH17/IL-23 immune fingerprint with the major orphan forms of ichthyosis and raise the possibility of IL-17–targeting strategies. |
|---|---|
| AbstractList | Background The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood. Objective We sought to characterize molecularly cutaneous inflammation and its correlation with clinical and barrier characteristics. Methods We analyzed biopsy specimens from 21 genotyped patients with ichthyosis (congenital ichthyosiform erythroderma, n = 6; lamellar ichthyosis, n = 7; epidermolytic ichthyosis, n = 5; and Netherton syndrome, n = 3) using immunohistochemistry and RT-PCR and compared them with specimens from healthy control subjects, patients with atopic dermatitis (AD), and patients with psoriasis. Clinical measures included the Ichthyosis Area Severity Index (IASI), which integrates erythema (IASI-E) and scaling (IASI-S); transepidermal water loss; and pruritus. Results Ichthyosis samples showed increased epidermal hyperplasia (increased thickness and keratin 16 expression) and T-cell and dendritic cell infiltrates. Increases of general inflammatory (IL-2), innate (IL-1β), and some TH1/interferon (IFN-γ) markers in patients with ichthyosis were comparable with those in patients with psoriasis or AD. TNF-α levels in patients with ichthyosis were increased only in those with Netherton syndrome but were much lower than in patients with psoriasis and those with AD. Expression of TH2 cytokines (IL-13 and IL-31) was similar to that seen in control subjects. The striking induction of IL-17-related genes or markers synergistically induced by IL-17 and TNF-α (IL-17A/C, IL-19, CXCL1, PI3, CCL20, and IL36G;P< .05) in patients with ichthyosis was similar to that seen in patients with psoriasis. IASI and IASI-E scores strongly correlated with IL-17A (r= 0.74,P< .001) and IL-17/TNF-synergistic/additive gene expression. These markers also significantly correlated with transepidermal water loss, suggesting a link between the barrier defect and inflammation in patients with ichthyosis. Conclusion Our data associate a shared TH17/IL-23 immune fingerprint with the major orphan forms of ichthyosis and raise the possibility of IL-17-targeting strategies. Background The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood. Objective We sought to characterize molecularly cutaneous inflammation and its correlation with clinical and barrier characteristics. Methods We analyzed biopsy specimens from 21 genotyped patients with ichthyosis (congenital ichthyosiform erythroderma, n = 6; lamellar ichthyosis, n = 7; epidermolytic ichthyosis, n = 5; and Netherton syndrome, n = 3) using immunohistochemistry and RT-PCR and compared them with specimens from healthy control subjects, patients with atopic dermatitis (AD), and patients with psoriasis. Clinical measures included the Ichthyosis Area Severity Index (IASI), which integrates erythema (IASI-E) and scaling (IASI-S); transepidermal water loss; and pruritus. Results Ichthyosis samples showed increased epidermal hyperplasia (increased thickness and keratin 16 expression) and T-cell and dendritic cell infiltrates. Increases of general inflammatory (IL-2), innate (IL-1 beta ), and some TH1/interferon (IFN- gamma ) markers in patients with ichthyosis were comparable with those in patients with psoriasis or AD. TNF- alpha levels in patients with ichthyosis were increased only in those with Netherton syndrome but were much lower than in patients with psoriasis and those with AD. Expression of TH2 cytokines (IL-13 and IL-31) was similar to that seen in control subjects. The striking induction of IL-17-related genes or markers synergistically induced by IL-17 and TNF- alpha (IL-17A/C, IL-19, CXCL1, PI3, CCL20, and IL36G; P < .05) in patients with ichthyosis was similar to that seen in patients with psoriasis. IASI and IASI-E scores strongly correlated with IL-17A (r = 0.74, P < .001) and IL-17/TNF-synergistic/additive gene expression. These markers also significantly correlated with transepidermal water loss, suggesting a link between the barrier defect and inflammation in patients with ichthyosis. Conclusion Our data associate a shared TH17/IL-23 immune fingerprint with the major orphan forms of ichthyosis and raise the possibility of IL-17-targeting strategies. BACKGROUNDThe ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood.OBJECTIVEWe sought to characterize molecularly cutaneous inflammation and its correlation with clinical and barrier characteristics.METHODSWe analyzed biopsy specimens from 21 genotyped patients with ichthyosis (congenital ichthyosiform erythroderma, n = 6; lamellar ichthyosis, n = 7; epidermolytic ichthyosis, n = 5; and Netherton syndrome, n = 3) using immunohistochemistry and RT-PCR and compared them with specimens from healthy control subjects, patients with atopic dermatitis (AD), and patients with psoriasis. Clinical measures included the Ichthyosis Area Severity Index (IASI), which integrates erythema (IASI-E) and scaling (IASI-S); transepidermal water loss; and pruritus.RESULTSIchthyosis samples showed increased epidermal hyperplasia (increased thickness and keratin 16 expression) and T-cell and dendritic cell infiltrates. Increases of general inflammatory (IL-2), innate (IL-1β), and some TH1/interferon (IFN-γ) markers in patients with ichthyosis were comparable with those in patients with psoriasis or AD. TNF-α levels in patients with ichthyosis were increased only in those with Netherton syndrome but were much lower than in patients with psoriasis and those with AD. Expression of TH2 cytokines (IL-13 and IL-31) was similar to that seen in control subjects. The striking induction of IL-17-related genes or markers synergistically induced by IL-17 and TNF-α (IL-17A/C, IL-19, CXCL1, PI3, CCL20, and IL36G; P < .05) in patients with ichthyosis was similar to that seen in patients with psoriasis. IASI and IASI-E scores strongly correlated with IL-17A (r = 0.74, P < .001) and IL-17/TNF-synergistic/additive gene expression. These markers also significantly correlated with transepidermal water loss, suggesting a link between the barrier defect and inflammation in patients with ichthyosis.CONCLUSIONOur data associate a shared TH17/IL-23 immune fingerprint with the major orphan forms of ichthyosis and raise the possibility of IL-17-targeting strategies. The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood. We sought to characterize molecularly cutaneous inflammation and its correlation with clinical and barrier characteristics. We analyzed biopsy specimens from 21 genotyped patients with ichthyosis (congenital ichthyosiform erythroderma, n = 6; lamellar ichthyosis, n = 7; epidermolytic ichthyosis, n = 5; and Netherton syndrome, n = 3) using immunohistochemistry and RT-PCR and compared them with specimens from healthy control subjects, patients with atopic dermatitis (AD), and patients with psoriasis. Clinical measures included the Ichthyosis Area Severity Index (IASI), which integrates erythema (IASI-E) and scaling (IASI-S); transepidermal water loss; and pruritus. Ichthyosis samples showed increased epidermal hyperplasia (increased thickness and keratin 16 expression) and T-cell and dendritic cell infiltrates. Increases of general inflammatory (IL-2), innate (IL-1β), and some T 1/interferon (IFN-γ) markers in patients with ichthyosis were comparable with those in patients with psoriasis or AD. TNF-α levels in patients with ichthyosis were increased only in those with Netherton syndrome but were much lower than in patients with psoriasis and those with AD. Expression of T 2 cytokines (IL-13 and IL-31) was similar to that seen in control subjects. The striking induction of IL-17-related genes or markers synergistically induced by IL-17 and TNF-α (IL-17A/C, IL-19, CXCL1, PI3, CCL20, and IL36G; P < .05) in patients with ichthyosis was similar to that seen in patients with psoriasis. IASI and IASI-E scores strongly correlated with IL-17A (r = 0.74, P < .001) and IL-17/TNF-synergistic/additive gene expression. These markers also significantly correlated with transepidermal water loss, suggesting a link between the barrier defect and inflammation in patients with ichthyosis. Our data associate a shared T 17/IL-23 immune fingerprint with the major orphan forms of ichthyosis and raise the possibility of IL-17-targeting strategies. The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood. We sought to characterize molecularly cutaneous inflammation and its correlation with clinical and barrier characteristics. We analyzed biopsy specimens from 21 genotyped patients with ichthyosis (congenital ichthyosiform erythroderma, n = 6; lamellar ichthyosis, n = 7; epidermolytic ichthyosis, n = 5; and Netherton syndrome, n = 3) using immunohistochemistry and RT-PCR and compared them with specimens from healthy control subjects, patients with atopic dermatitis (AD), and patients with psoriasis. Clinical measures included the Ichthyosis Area Severity Index (IASI), which integrates erythema (IASI-E) and scaling (IASI-S); transepidermal water loss; and pruritus. Ichthyosis samples showed increased epidermal hyperplasia (increased thickness and keratin 16 expression) and T-cell and dendritic cell infiltrates. Increases of general inflammatory (IL-2), innate (IL-1β), and some TH1/interferon (IFN-γ) markers in patients with ichthyosis were comparable with those in patients with psoriasis or AD. TNF-α levels in patients with ichthyosis were increased only in those with Netherton syndrome but were much lower than in patients with psoriasis and those with AD. Expression of TH2 cytokines (IL-13 and IL-31) was similar to that seen in control subjects. The striking induction of IL-17–related genes or markers synergistically induced by IL-17 and TNF-α (IL-17A/C, IL-19, CXCL1, PI3, CCL20, and IL36G; P < .05) in patients with ichthyosis was similar to that seen in patients with psoriasis. IASI and IASI-E scores strongly correlated with IL-17A (r = 0.74, P < .001) and IL-17/TNF–synergistic/additive gene expression. These markers also significantly correlated with transepidermal water loss, suggesting a link between the barrier defect and inflammation in patients with ichthyosis. Our data associate a shared TH17/IL-23 immune fingerprint with the major orphan forms of ichthyosis and raise the possibility of IL-17–targeting strategies. Background The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is largely lacking because the underlying molecular basis is poorly understood. Objective We sought to characterize molecularly cutaneous inflammation and its correlation with clinical and barrier characteristics. Methods We analyzed biopsy specimens from 21 genotyped patients with ichthyosis (congenital ichthyosiform erythroderma, n = 6; lamellar ichthyosis, n = 7; epidermolytic ichthyosis, n = 5; and Netherton syndrome, n = 3) using immunohistochemistry and RT-PCR and compared them with specimens from healthy control subjects, patients with atopic dermatitis (AD), and patients with psoriasis. Clinical measures included the Ichthyosis Area Severity Index (IASI), which integrates erythema (IASI-E) and scaling (IASI-S); transepidermal water loss; and pruritus. Results Ichthyosis samples showed increased epidermal hyperplasia (increased thickness and keratin 16 expression) and T-cell and dendritic cell infiltrates. Increases of general inflammatory (IL-2), innate (IL-1β), and some TH 1/interferon (IFN-γ) markers in patients with ichthyosis were comparable with those in patients with psoriasis or AD. TNF-α levels in patients with ichthyosis were increased only in those with Netherton syndrome but were much lower than in patients with psoriasis and those with AD. Expression of TH 2 cytokines (IL-13 and IL-31) was similar to that seen in control subjects. The striking induction of IL-17–related genes or markers synergistically induced by IL-17 and TNF-α (IL-17A/C, IL-19, CXCL1, PI3, CCL20, and IL36G; P < .05) in patients with ichthyosis was similar to that seen in patients with psoriasis. IASI and IASI-E scores strongly correlated with IL-17A ( r = 0.74, P < .001) and IL-17/TNF–synergistic/additive gene expression. These markers also significantly correlated with transepidermal water loss, suggesting a link between the barrier defect and inflammation in patients with ichthyosis. Conclusion Our data associate a shared TH 17/IL-23 immune fingerprint with the major orphan forms of ichthyosis and raise the possibility of IL-17–targeting strategies. |
| Author | Zheng, Xiuzhong Oliva, Margeaux Kunjravia, Norma Renert-Yuval, Yael Suprun, Maria Ungar, Benjamin Friedland, Rivka Guttman-Yassky, Emma Paller, Amy S. Estrada, Yeriel D. Choate, Keith A. Suárez-Fariñas, Mayte Esaki, Hitokazu Huynh, Thy Nhat Peng, Xiangyu Krueger, James G. |
| AuthorAffiliation | 6 Icahn Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA 4 Laboratory for Investigative Dermatology, Rockefeller University, New York, NY 10065, USA 2 Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 3 Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA 5 Department of Dermatology, Yale University School of Medicine, New Haven, CT 06520, USA 1 Departments of Dermatology and Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA |
| AuthorAffiliation_xml | – name: 4 Laboratory for Investigative Dermatology, Rockefeller University, New York, NY 10065, USA – name: 1 Departments of Dermatology and Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA – name: 2 Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 6 Icahn Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA – name: 3 Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA – name: 5 Department of Dermatology, Yale University School of Medicine, New Haven, CT 06520, USA |
| Author_xml | – sequence: 1 givenname: Amy S. surname: Paller fullname: Paller, Amy S. email: apaller@northwestern.edu organization: Departments of Dermatology and Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, Ill – sequence: 2 givenname: Yael surname: Renert-Yuval fullname: Renert-Yuval, Yael organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 3 givenname: Maria surname: Suprun fullname: Suprun, Maria organization: Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 4 givenname: Hitokazu orcidid: 0000-0002-3716-520X surname: Esaki fullname: Esaki, Hitokazu organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 5 givenname: Margeaux surname: Oliva fullname: Oliva, Margeaux organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 6 givenname: Thy Nhat surname: Huynh fullname: Huynh, Thy Nhat organization: Departments of Dermatology and Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, Ill – sequence: 7 givenname: Benjamin surname: Ungar fullname: Ungar, Benjamin organization: Laboratory for Investigative Dermatology, Rockefeller University, New York, NY – sequence: 8 givenname: Norma orcidid: 0000-0003-0308-1048 surname: Kunjravia fullname: Kunjravia, Norma organization: Laboratory for Investigative Dermatology, Rockefeller University, New York, NY – sequence: 9 givenname: Rivka orcidid: 0000-0001-8117-3656 surname: Friedland fullname: Friedland, Rivka organization: Departments of Dermatology and Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, Ill – sequence: 10 givenname: Xiangyu surname: Peng fullname: Peng, Xiangyu organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 11 givenname: Xiuzhong surname: Zheng fullname: Zheng, Xiuzhong organization: Laboratory for Investigative Dermatology, Rockefeller University, New York, NY – sequence: 12 givenname: Yeriel D. surname: Estrada fullname: Estrada, Yeriel D. organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 13 givenname: James G. surname: Krueger fullname: Krueger, James G. organization: Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 14 givenname: Keith A. surname: Choate fullname: Choate, Keith A. organization: Department of Dermatology, Yale University School of Medicine, New Haven, Conn – sequence: 15 givenname: Mayte surname: Suárez-Fariñas fullname: Suárez-Fariñas, Mayte organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY – sequence: 16 givenname: Emma surname: Guttman-Yassky fullname: Guttman-Yassky, Emma organization: Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27554821$$D View this record in MEDLINE/PubMed |
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| Snippet | The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy is... Background The ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based... BACKGROUNDThe ichthyoses are rare genetic disorders associated with generalized scaling, erythema, and epidermal barrier impairment. Pathogenesis-based therapy... |
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| SubjectTerms | Adolescent Adult Age Aged Allergy and Immunology autosomal recessive congenital ichthyosis Baldness Child Congenital diseases congenital ichthyosiform erythroderma Cytokines Demographics Dermatitis, Atopic - genetics Dermatitis, Atopic - immunology Epidermis epidermolytic ichthyosis Family medical history Female Gene Expression Humans ichthyosis Ichthyosis - genetics Ichthyosis - immunology IL-17 Inflammation Interleukin-17 - genetics Interleukin-17 - immunology Interleukin-23 - genetics Interleukin-23 - immunology lamellar ichthyosis Male Middle Aged Mutation Netherton syndrome Pruritus Psoriasis Psoriasis - genetics Psoriasis - immunology RNA, Messenger - metabolism Severity of Illness Index Skin Skin - immunology TNF-α Young Adult |
| Title | An IL-17–dominant immune profile is shared across the major orphan forms of ichthyosis |
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