Autoimmunity and autoimmune co‐morbidities in psoriasis

Kazuhisa Furue; Takamichi Ito; Gaku Tsuji; Takafumi Kadono; Takeshi Nakahara; Masutaka Furue

doi:10.1111/imm.12891

. 2018 Feb 6;154(1):21–27. doi: 10.1111/imm.12891

Autoimmunity and autoimmune co‐morbidities in psoriasis

Kazuhisa Furue ¹, Takamichi Ito ¹, Gaku Tsuji ¹, Takafumi Kadono ², Takeshi Nakahara ^1,³, Masutaka Furue ^1,^3,^✉

PMCID: PMC5904708 PMID: 29315555

Summary

Psoriasis is characterized by widespread scaly erythematous plaques that cause significant physical and psychological burdens for the affected individuals. Accelerated inflammation driven by the tumour necrosis factor‐α/interleukin‐23/interleukin‐17 axis is now known to be the major mechanism in the development of psoriasis. In addition, psoriasis has an autoimmune nature that manifests as autoreactive T cells and is co‐morbid with other autoimmune diseases, such as autoimmune bullous diseases, vitiligo, alopecia and thyroiditis. In this article, we review the recent topics on autoimmunity and autoimmune co‐morbidities in psoriasis.

Keywords: alopecia, autoimmunity, bullous pemphigoid, psoriasis, thyroiditis, vitiligo

Introduction

Psoriasis is a chronic, immune‐mediated, inflammatory skin disorder that affects approximately 0·1–3% of the general population worldwide.1, 2, 3 Given the visible nature of skin lesions, including those on the face, scalp, hands and nails,4, 5, 6, 7 psoriasis is a significant physical and psychological burden to afflicted patients, decreases patient quality of life, and induces feelings of internalized stigma.8, 9, 10, 11, 12

The disease burden of psoriasis is further increased by its association with psoriatic arthritis, which is characterized by seronegative spondyloarthropathies, enthesitis and elevated C‐reactive protein levels.1, 13, 14, 15, 16 Approximately 15–30% of Caucasians with psoriasis eventually develop psoriatic arthritis.17 Although the prevalence is lower in Asian populations (Chinese 5·3–7·3%, Japanese 10·5% and Korean 11·2%), psoriatic arthritis significantly hampers patients’ daily lives.16, 17 Additionally, psoriasis has significant co‐morbidity with systemic inflammatory diseases, such as cardiovascular diseases and metabolic syndrome, and these conditions are currently receiving increasing attention.18, 19, 20, 21, 22, 23, 24, 25, 26, 27 In parallel, a plethora of inflammatory biomarkers are elevated in psoriasis.28, 29, 30, 31, 32

In addition to these co‐morbid diseases that have a systemic inflammatory nature,33 psoriasis presents with autoimmune aspects and co‐exists with a variety of autoimmune disorders.34, 35, 36, 37, 38, 39 In this article, we summarize recent topics on autoimmunity and autoimmune co‐morbidities in psoriasis.

Current pathogenesis of psoriasis and its treatments

Pathogenesis of psoriasis is multifactorial, including environmental,40, 41, 42 genetic43, 44 and immune‐related factors.45, 46, 47, 48, 49 Recent genome‐wide association studies have identified numerous risk‐associated variants within 44 susceptibility loci for psoriasis, including HLAC*06:02, LCE3D, IL23R and CARD14.1, 43, 44, 50, 51, 52 These susceptibility genes are predominantly related to the innate and adaptive immune system as well as to skin barrier function.1, 43, 44

Cutaneous trauma, such as incisional injury, induces the expression of functional cathelicidin at the injured site.53 Cathelicidin (LL37) is one of the anti‐microbial peptides that are produced by keratinocytes and neutrophils.53 An initial trigger of psoriasis is believed to involve activation of plasmacytoid dendritic cells (DCs) upon stimulation by complexes of host DNA and LL37.45, 46, 47, 48 Activated plasmacytoid DCs and damaged keratinocytes produce interferon‐α (IFN‐α), IFN‐β and tumour necrosis factor‐α (TNF‐α), which result in further production of TNF‐α and interleukin‐23 (IL‐23) by plasmacytoid and recruited inflammatory DCs [TNF/inducible nitric oxide synthase‐producing DCs (TIP‐DCs)].45, 46, 47, 48 Interleukin‐23 is critically involved in the generation and activation of IL‐17‐ and IL‐22‐producing effector T helper type 17 (Th17) and Th22 cells.48, 49

Interleukin‐17 up‐regulates the proliferation of keratinocytes and down‐regulates their differentiation.54 Interleukin‐22 also drives epidermal hyperplasia, primarily by down‐regulation of genes involved in terminal differentiation.55, 56 Interleukin‐17 acts on keratinocytes to induce chemokines that lead to neutrophil, TIP‐DC and Th17 cell influx into the skin;57 and up‐regulates production of the neutrophil‐attractive chemokines CXCL1, CXCL2 and CXCL8 by keratinocytes.58, 59, 60

The accelerated TNF‐α/IL‐23/IL‐17 axis coincides with the characteristic histopathology of psoriasis, such as epidermal hyperproliferation, aberrant differentiation and neutrophilic microabscess. Regarding treatments, topical application of steroids and vitamin D3 analogues inhibits psoriatic inflammation and normalizes epidermal differentiation.61, 62, 63, 64, 65 Systemic treatments, such as cyclosporine, methotrexate and the phosphodiesterase 4 inhibitor apremilast, are useful for patients with extensive lesions.66, 67, 68 Clinical trials have demonstrated the efficacy of the oral janus kinase inhibitor tofacitinib for psoriasis.69, 70 Biological agents targeting TNF‐α, IL‐23 and IL‐17 signalling exhibit high efficacy for patients with severe lesions, arthritis or disturbed quality of life.71, 72, 73, 74, 75, 76, 77, 78, 79 However, development of the anti‐IL‐22 antibody fezakinumab (ILV‐094) has been discontinued due to treatment failure, probably because of the redundancy of IL‐22 in humans.48 The biologicals are applicable in both paediatric and elderly patients, in patients undergoing haemodialysis and patients with perioperational circumstances.80, 81, 82, 83 They are also used in pregnant women, although their safety warrants further evaluation.84, 85 Switching of biologicals is recommended for patients with primary failure, secondary failure and infusion reactions.86

Genetic backgrounds are also related to the treatment response to biologicals.87, 88 The high cost of biologicals limits access to these medications; however, cost‐saving biosimilars are rapidly advancing to the market worldwide.89, 90, 91 Biologicals are effective not only for psoriasis but also for co‐morbid cardiovascular and metabolic diseases.92, 93 In addition, monitoring of infection is mandatory to avoid serious consequences.94, 95, 96 The emergence of antidrug antibodies is another important issue that reduces the treatment response and promotes treatment failure during biological therapy.97, 98

Autoimmunity in psoriasis

In addition to the TNF‐α/IL‐23/IL‐17‐shifted immune deviation, psoriasis is likely to be associated with an autoimmune background.34, 35 Several studies have revealed the presence of autoreactive T cells in psoriasis (Fig. 1).99, 100, 101

Based on clear‐cut effectiveness of biologicals, the tumour necrosis factor‐α (TNF‐α)/ interleukin‐23 (IL‐23)/ IL‐17A/ IL‐22 axis plays a major role in the pathogenesis of psoriasis. In addition, psoriasis possesses an autoimmune nature manifesting autoreactive T cells that are frequently restricted to HLA‐C*06:02. Psoriasis is also co‐morbid with other autoimmune diseases, such as bullous pemphigoid, vitiligo, alopecia and thyroiditis.

Exacerbation of chronic psoriasis can be associated with streptococcal throat infections.99, 100 Lesional skin and tonsils of patients with psoriasis harbour T cells co‐reactive to streptococcal M protein and type I keratin.99, 100 Streptococcal M protein exhibits structural homology with type I keratins in epidermal keratinocytes.100 These co‐reactive T cells elicited by molecular mimicry are cutaneous lymphocyte antigen (CLA)⁺, CD8⁺ and IL‐17 producers.100 The co‐reactive T cells may be pathogenic because tonsillectomy improves clinical symptoms in concert with a significant reduction of this T‐cell population.100 Type I keratin‐specific T cells are also reported in psoriasis by another research group.101

The antimicrobial peptide LL37 is over‐expressed in psoriatic epidermis.46, 101, 102 LL37 not only triggers the TNF‐α/IL‐23/IL‐17 axis by activating DCs but also works as an autoantigen to activate the T‐cell adaptive immune system.46, 101, 102 LL37 is recognized as an autoantigen by circulating T cells in 46% of psoriasis patients and more frequently (75%) in moderate‐to‐severe psoriasis.101 In 54% of LL37‐responder patients, LL37‐specific T cells are exclusively CD4⁺, 29% are both CD4⁺ and CD8⁺, and 17% are exclusively CD8⁺. These LL37‐specific T cells express CLA and produce variable amounts of IFN‐γ, IL‐17 and IL‐22 but not IL‐4. The frequency of LL37‐specific T cells is significantly correlated with disease severity and is reduced by anti‐TNF‐α therapy.101

The pivotal role of intra‐epidermal CD8⁺ T cells has been documented in psoriasis.103, 104, 105, 106 These intra‐epidermal CD8⁺ T cells produce pathogenic IL‐17A, and neutralization of CD8⁺ T cells effectively prevents psoriasis development in xenotransplanted mice models in vivo.105 Moreover, a recent study by Arakawa et al.106 demonstrated that intraepidermal CD8⁺ T cells recognize ADAMTS‐like protein 5 (ADAMTSL5) on melanocytes in concert with HLA‐C*06:02, which is the main psoriasis risk allele. Of note, LL37‐specific CD8⁺ T cells are also restricted to HLAC*06:02.101

In addition to the autoreactive T‐cell response, several autoantibodies have been demonstrated in patients with psoriasis, including anti‐stratum corneum antibody,107 anti‐squamous cell carcinoma antigen108 and anti‐heatshock protein 65.109 However, the clinical significance of the autoantibody production remains elusive.

HLA class I and class II polymorphisms are associated with immune‐mediated diseases typically in a disease‐specific manner.110, 111 Among susceptibility genes in psoriasis, HLAC*06:02 has a fundamental importance and defines familial clustering, early onset and a more severe course of psoriasis.112, 113 The fact that patients with psoriasis harbour autoreactive T cells that are restricted to HLAC*06:02 stress a potential role for these T cells in the development and perpetuation of psoriasis.

Intriguingly, the occurrence of psoriasis is commonly noted in human immunodeficiency virus (HIV) infection.114, 115, 116, 117, 118 Psoriasis with HIV infection may have a more severe course with sudden exacerbations and may be refractory to treatment.114, 115, 116, 117, 118 Paradoxical onset of psoriasis and arthritis is also demonstrated in patients treated with biologicals.119, 120 Anti‐TNF‐α antibodies frequently induce increased levels of KL‐6, which is a serum marker for interstitial pneumonia.121 In addition, the onset and exacerbation of psoriasis have been reported in melanoma patients treated with the anti‐programmed cell death protein 1 antibody nivolumab.122, 123 These phenomena may be related to a disruption in cytokine balance following treatment with biologicals, resulting in the up‐regulation of plasmacytoid DCs and the subsequent production of unopposed IFNs, leading to the bypassed IL‐17 over‐production.124

Autoimmune diseases co‐morbid with psoriasis

Consistent with the autoimmune nature of psoriasis, numerous other autoimmune diseases, including autoimmune bullous diseases,125 vitiligo,126 alopecia127 and thyroiditis,128 are co‐morbid with psoriasis. Among them, autoimmune bullous diseases, such as bullous pemphigoid and anti‐laminin γ1 (p200) pemphigoid, are consistently documented.37, 125, 129, 130 In a nationwide population‐based study of 3485 patients with bullous pemphigoid and 17425 matched controls, psoriasis is significantly associated with bullous pemphigoid [odds ratio (OR) 2·02; 95% CI 1·54–2·66].130 In a case–control study of 287 patients with bullous pemphigoid and 1373 matched controls, the prevalence rate of psoriasis is greater in patients with bullous pemphigoid compared with control subjects (OR 4·4; 95% CI 2·2–8·9).125 This association is also significant among both sexes.125 In a case series of coexisting psoriasis and autoimmune bullous diseases, bullous pemphigoid is the most prevalent (63·4%) followed by anti‐laminin γ1 pemphigoid (37·2%).129

Vitiligo is an autoimmune hypopigmentation disorder that is associated with psoriasis. Arunachalam et al.126 reported that 27 of 463 (5·8%) patients with vitiligo have co‐morbid psoriasis. A cross‐sectional study of 1925 children and adolescents with psoriasis and 1 194 712 controls without psoriasis reveals a strong association of vitiligo with psoriasis (adjusted OR 4·76; 95% CI 1·71–13·20).131 A significant association of vitiligo is evident in a nationwide study including 51 800 psoriasis patients with an OR of 5·94 (95% CI 3·79–9·31).132 In parallel, it is interesting that vitiligo and psoriasis share a common genetic susceptible locus (rs9468925 in HLA‐C/HLA‐B).133

Psoriasis is also associated with autoimmune hair loss, namely alopecia areata (OR 4·71; 95% CI 2·98–7·45), in a national database in Taiwan.132 In a cohort study including 25 341 patients with psoriasis, a significant association of alopecia areata and psoriasis was also noted (OR 2·5; 95% CI 2·0–3·0).127

Hashimoto's thyroiditis and thyroid autoimmunity are frequently observed in the general population.134 Free thyroxin levels are significantly increased in 105 psoriasis patients without arthritis compared with control 96 patients with tinea pedis.135 In a hospital‐based cross‐sectional study of 856 615 patients, 9615 patients were diagnosed with psoriasis, and 1745 patients had Hashimoto's thyroiditis. A significant association exists for psoriasis and Hashimoto's thyroiditis even after adjusting for confounding variables, including gender, age, psoriatic arthropathy and the use of systemic anti‐psoriatic agents (OR 2·49; 95% CI 1·79–3·48).128 However, Vassilatou et al.136 did not identify any tendency of association between psoriasis and autoimmune thyroiditis in their 114 patients with psoriasis.

Although the precise mechanisms underlying the autoimmune co‐morbidities are not completely understood, damage to the basement membrane, melanocytes and hairs by chronic psoriatic inflammation may initiate and accelerate skin‐related autoimmune diseases. An association of Crohn's disease and collagen diseases, such as systemic lupus erythematosus, rheumatoid arthritis, Sjögren's syndrome and systemic sclerosis, has been demonstrated in psoriasis patients.127, 137, 138 Some patients with psoriasis develop collagen diseases upon treatment with biologicals.139, 140, 141

Similar to psoriasis, IFNs, DNA–LL‐37 complex and plasmacytoid DCs play a pivotal role in triggering and perpetuating systemic lupus erythematosus.142, 143, 144 Interferons accelerate the formation of DNA–LL37 complex that activates plasmacytoid DCs to produce high levels of IFNs and IL‐23.142, 144 Interleukin‐23 induces IL‐17 production, which promotes autoimmunity.144 Crohn's disease is also deeply linked to TNF‐α/IL‐23 signalling because both anti‐TNF‐α and anti‐IL‐23 biologicals are effective in this disease.145, 146 In vitiligo, IFN signature is also involved in the initiation of its immune response with the activation of plasmacytoid DCs.147 Serum levels of IL‐23 are also elevated in vitiligo.148 These results supports a notion that common pathogenic pathways or shared autoantigens exist in psoriasis and other autoimmune diseases.

Conclusion

Psoriasis is a common chronic inflammatory skin disease that significantly decreases the physical and psychological quality of life of afflicted patients. The underlying inflammatory process results in increased co‐morbidity with systemic inflammatory diseases, such as cardiovascular diseases and metabolic syndrome. In addition, numerous pathogenic traits are shared by psoriasis and other autoimmune diseases, such as autoimmune bullous diseases, vitiligo and alopecia areata. Future studies are warranted to explore the distinct pathways that underpin the inflammatory and autoimmune co‐morbidity.

Disclosures

The authors declare that they have no conflict of interest.

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PERMALINK

Autoimmunity and autoimmune co‐morbidities in psoriasis

Kazuhisa Furue

Takamichi Ito

Gaku Tsuji

Takafumi Kadono

Takeshi Nakahara

Masutaka Furue

Summary

Introduction

Current pathogenesis of psoriasis and its treatments

Autoimmunity in psoriasis

Figure 1.

Autoimmune diseases co‐morbid with psoriasis

Conclusion

Disclosures

References

ACTIONS

PERMALINK

RESOURCES

Cite

Add to Collections

PERMALINK

Autoimmunity and autoimmune co‐morbidities in psoriasis

Kazuhisa Furue

Takamichi Ito

Gaku Tsuji

Takafumi Kadono

Takeshi Nakahara

Masutaka Furue

Summary

Introduction

Current pathogenesis of psoriasis and its treatments

Autoimmunity in psoriasis

Figure 1.

Autoimmune diseases co‐morbid with psoriasis

Conclusion

Disclosures

References

ACTIONS

PERMALINK

RESOURCES

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