Review Article
Medical Progress
Psoriasis
N Engl J Med 2005; 352:1899-1912May 5, 2005
- Article
Psoriasis, a common inflammatory skin disorder, has received attention as a target for new pathogenesis-oriented biologic therapies. In this article, we review the genetic, clinical, and pathogenic aspects of psoriasis and discuss their implications for new therapies.
Epidemiologic and Genetic Features
Though psoriasis is a common skin disease, its definition by Ferdinand von Hebra as a distinct entity dates back only to the year 1841, and estimates of its prevalence — around 2 percent, according to standard textbooks — stem from only a few population-based studies. Perhaps the most comprehensive field study was performed in the Faroe Islands, where 2.8 percent of the inhabitants were reported to be affected.1 This prevalence rate is higher than that in central Europe, where prevalence is approximately 1.5 percent, according to a more recent analysis.2 Ethnic factors also appear to influence the prevalence of psoriasis, which ranges from no cases in the Samoan population to 12 percent in Arctic Kasach'ye.2 The influence of ethnic factors is particularly evident when one compares prevalence rates within the United States. The prevalence among blacks (0.45 to 0.7 percent)3 is far lower than that in the remainder of the U.S. population (1.4 to 4.6 percent).4
Numerous family studies have provided compelling evidence of a genetic predisposition to psoriasis, although the inheritance pattern is still unclear.5 The illness develops in as many as half of the siblings of persons with psoriasis when both parents are affected, but prevalence falls to 16 percent when only one parent has psoriasis and to 8 percent when neither parent is affected.6 The concordance rate for monozygotic twins is around 70 percent, as compared with some 20 percent for dizygotic twins, a finding that further supports the concept of genetic predisposition.7,8 As many as 71 percent of patients with childhood psoriasis have a positive family history.9
Within the past decade, several putative loci for genetic susceptibility to the disease have been reported on the basis of genome-wide linkage studies, but there has not been widespread replication of the results — a problem that has also been encountered in the investigation of other complex diseases.10,11 However, one locus in the major-histocompatibility-complex (MHC) region on chromosome 6 has been replicated in several populations12,13 (see Glossary for definitions of terms). This locus, termed psoriasis susceptibility 1 (PSORS1), is considered the most important susceptibility locus. On the basis of association studies of three tightly linked susceptibility alleles (HLA-Cw6,14 HCR*WWCC, 15 and the HLA-associated S gene16), PSORS1 appears to be associated with up to 50 percent of cases of psoriasis. Other susceptibility loci are located on chromosomes 17q25 (PSORS2),17 4q34 (PSORS3),18 1q (PSORS4),19 3q21 (PSORS5),20 19p13 (PSORS6),21 and 1p (PSORS7).22 Most recently, an additional gene locus for psoriasis susceptibility has been discovered on chromosome 17q25.23 This locus, a runt-related transcription factor 1 (RUNX1) binding-site variant, encodes for a gene involved in the development of blood cells, including those of the immune system.
Clinical and Histopathological Features
People with psoriasis typically have sharply demarcated chronic erythematous plaques covered by silvery white scales, which most commonly appear on the elbows, knees, scalp, umbilicus, and lumbar area (Figure 1A to Figure 1DFigure 1
Clinical Features of Psoriasis.). An inverse type of psoriasis spares these sites and instead appears in intertriginous areas, where scaling is minimal (Figure 1E). Eruptive guttate psoriasis, which may be the initial manifestation of the disease and is often preceded by streptococcal infection by two to three weeks,24 exhibits small, disseminated erythematosquamous papules and plaques (Figure 1B). Psoriatic diaper rash appears to be the most common type of psoriasis in children under the age of two years.9 In addition to small pustules that may occur in lesions of psoriasis vulgaris, various forms of pustular psoriasis have been described (Figure 1F). Generalized pustular psoriasis (Figure 1G) is characterized by disseminated deep-red erythematous areas and pustules, which may merge to extensive lakes of pus. In contrast, there are two localized variants termed palmoplantar pustulosis and acrodermatitis continua suppurativa (Figure 1H, depicting onychodystrophy in the latter condition). Despite its wider clinical spectrum, pustular psoriasis is quite rare as compared with nonpustular forms. Both pustular and the more common vulgar forms may progress to psoriatic erythroderma affecting the entire body surface (Figure 1C).
Psoriatic arthritis is an extracutaneous manifestation that affects at least 5 percent and perhaps as many as 20 percent of patients with psoriasis (Figure 1I).25,26 The nails are affected in the majority of patients with psoriatic arthritis, but nail involvement can be seen in all types of psoriasis. The fingernails are more frequently affected than are toenails (on average, in 50 percent of patients as compared with 35 percent), and lesions range from pits and yellowish discoloration (Figure 1J and Figure 1K) to severe onychodystrophy, a typical complication of acrodermatitis continua suppurativa (Figure 1H).25,26
For many patients, the symptoms of psoriasis improve in the summer and worsen in the winter, reflecting the well-established notion that the course of the disease is influenced by various environmental factors. Physical trauma may trigger psoriatic lesions at sites of injury (Koebner's phenomenon), possibly through the release of proinflammatory cytokines, the unmasking of autoantigens, or both.27 In fact, some treatments for psoriasis that have proinflammatory potential (e.g., anthralin and phototherapy) appear to trigger psoriasis if applied too aggressively — for example, in high initial doses.
Molecular mechanisms underlying drug-induced flares of psoriasis are incompletely understood. Mechanisms for certain medications are partially delineated. For example, beta-adrenergic blockers may induce epidermal hyperproliferation associated with a decrease of intraepidermal cyclic AMP; lithium may elevate proinflammatory cytokines, thereby stimulating cutaneous leukocyte recruitment; and chloroquine blocks epidermal transglutaminase, an enzyme that is pivotally involved in the terminal differentiation of keratinocytes.28
Infections, particularly streptococcal infections of the upper respiratory tract, have long been recognized as triggers of psoriasis.24 In addition, exacerbation or even initial manifestation of psoriasis has been observed in patients infected with the human immunodeficiency virus (HIV). However, because of clinical similarities, psoriasis in patients with HIV infection may be misinterpreted as seborrheic eczema.29
Psoriatic skin exhibits pathological changes in most, if not all, cutaneous cell types. The typical erythematosquamous plaque contains histopathological hallmark features that include hyperproliferation of epidermal keratinocytes and hyperkeratosis, as well as infiltration of immunocytes along with angiogenesis, with resultant typical thickening and scaling of the erythematous skin. Mitotic activity of basal keratinocytes is increased by as much as a factor of 50 in psoriatic skin, so keratinocytes need only 3 to 5 days in order to move from the basal layer to the cornified layer (instead of the normal 28 to 30 days). This dramatically shortened maturation time is accompanied by altered differentiation, reflected by the focal absence of the granular layer of the epidermis and parakeratosis, or nuclei still present in the thickened cornified layer (Figure 2A through 2DFigure 2
Complex Pathological Tissue Alterations in Psoriatic Skin.).Psoriatic epidermis demonstrates aberrant expression of antigens associated with hyperproliferation, such as the heterodimer keratin 6–keratin 16 and heat-shock proteins. In addition, induced expression of MHC class II antigens and intercellular adhesion molecule 1 (ICAM-1) is observed.4,30 These molecules are involved in interactions with lymphocytes such as adhesion or antigen recognition (Figure 2E). Moreover, vascular endothelial cells are primed to take part in angiogenesis in psoriasis, and blood vessels that are associated with psoriatic lesions become dilated and contorted, reaching directly beneath the epidermis in the dermal papillar regions (Figure 2B). The involved vascular endothelial cells express increased levels of ICAM-1 (CD54), E-selectin (CD62E), vascular-cell adhesion molecule 1 (CD106), and MHC class II antigens, indicating activation.31 Then a mixed inflammatory infiltrate that contains activated CD3+ T lymphocytes within both the dermis and epidermis is evident (Figure 2F),32 within which CD4+ T cells are distributed randomly. In contrast, the majority of CD8+ T cells, some of which express epithelial-specific adhesion receptors (Figure 2G),33 reside preferentially within the epidermis.34
Many T cells within psoriatic skin exhibit an activated phenotype characterized by increased expression of costimulatory molecules such as CD2, adhesion molecules including leukocyte-function–associated antigen 1 (LFA-1) and cutaneous lymphocyte-associated antigen (CLA), or the high-affinity interleukin-2 receptor. Neutrophils localize to the dermis, migrate focally into the epidermis, and form Munro microabscesses, which become translocated upward within the epidermal stratum corneum (Figure 2C and Figure 2D).35 In addition, psoriatic skin contains an increased number of dermal mast cells and dendritic cells.36
Immunopathogenesis
Psoriasis is an instructive model for studying interactions of immigrating immunocytes with resident epithelial and mesenchymal cells. This disease vividly highlights the pathogenic importance of T cells and simultaneously illustrates how advances in our understanding of molecular immune mechanisms can be translated into innovative therapies.
Although many factors that contribute to the generation of psoriatic lesions remain obscure, compelling circumstantial and experimental evidence suggests a primary T-lymphocyte–based immunopathogenesis (Figure 3Figure 3
Putative T-Cell Responses in the Pathogenesis of a Psoriatic Lesion.).30 The response of psoriasis to treatment with compounds that act on lymphocytes, such as cyclosporine, first described for use in psoriasis in 1979, is an early example.38 More recently, other compounds specifically targeting T-cell functions were found to alleviate psoriasis. These include interleukin-2 fused to truncated diphtheria toxin (DAB389IL-2)39 and antibodies directed against CD2,40 CD11a,41,42 or, in some cases, CD4.43,44 In addition, there is a possible linkage of the psoriasis-susceptibility gene PSORS2 with a gene involved in the regulation of interleukin-2.17 Furthermore, psoriasis may not recur after bone marrow transplantation (performed in order to treat disorders unrelated to psoriasis) from healthy donors45 or may develop for the first time after bone marrow transplantation from a donor with psoriasis.46 The aforementioned association of psoriasis with certain MHC alleles — such as HLA-B13, HLA-B17, HLA-Bw57, and HLA-Cw6 — also suggests a pathogenic role of T cells.4 Indeed, some investigators have reported that there is a restricted use of T-cell receptor variable genes within psoriatic lesions, a finding that implies antigen-specific T-cell responses.47 Although the pathogenic relevance of this oligoclonal T-cell expansion is not entirely clear,48 it is possible that the failure to demonstrate oligoclonality in some cases of psoriasis is due, at least in part, to the colonization of psoriatic lesions by bacteria that produce superantigen, triggering the T-cell receptor without using the variable antigen-recognition sites.49 The permissive role of bacterial superantigens in the pathogenesis of psoriasis is well established.49 In addition, sequence similarities between streptococcal M peptides and human keratins, such as keratin 17, led to the hypothesis that keratinocyte proteins function as autoantigens in psoriasis.50 The generation of psoriasis-like skin lesions has been described in animal models, by a process based on T-cell dysregulation without prior epithelial abnormalities.51,52 In addition, the role of T lymphocytes as key effector cells is strongly supported by work from various groups in xenotransplantation models. Injection of activated T lymphocytes from patients with psoriasis into unaffected skin transplanted from the same patients onto SCID (severe combined immunodeficiency) mice resulted in the generation of psoriatic lesions in the animals.53-55 Although additional rodent models support the prominent role of T lymphocytes, it is also clear that these T lymphocytes can trigger the disease only in a susceptible environment, since these results are obtained with skin from psoriatic, but not from healthy, donors.56
Cytokines, Chemokines, and Adhesion Molecules
Psoriasis may serve as a model of a disease that clearly shows the central role of cytokines and chemokines and the functional interaction of these proteins with adhesion molecules in the recruitment of tissue-specific lymphocytes.57,58 Cytokine dysregulation may explain, at least in part, the complex tissue alterations in psoriasis (Figure 4Figure 4
The Cytokine and Chemokine Network.). Proinflammatory cytokines59-62 induce the expression of adhesion molecules on endothelial cells and keratinocytes, allowing them to interact with leukocytes. This results in leukocyte extravasation at the site of inflammation, along with migration through the cutaneous matrix toward the epidermis.63,64 Numerous studies have identified tumor necrosis factor α (TNF-α) as a particularly relevant cytokine regulating this complex inflammatory cascade. Its key role is underlined by the therapeutic efficacy of compounds that interfere with TNF-α functions.41,65,66 Psoriatic skin is further characterized by increased angioneogenesis in a milieu rich in proangiogenic factors.31,67 Complementary to the up-regulation of proinflammatory cytokines, reduced levels of the antiinflammatory cytokine interleukin-10, along with the relative dominance of type 1 helper T (Th1) cytokines, such as interferon-γ and interleukin-2, add to a milieu with mediator imbalance.68-70 The exact mechanisms by which these cytokines regulate the microenvironment that influences psoriasis need further clarification.Recent evidence strongly suggests that chemokines are pivotal for the trafficking and compartmentalization of leukocytes in the psoriatic disease process (Figure 4).58,71 The effector-T-cell population that is putatively the most relevant in psoriasis is characterized by the expression of skin-homing receptor CLA and the CC chemokine receptor 4 (CCR4).72 Other chemokines that are implicated in the recruitment of T cells into psoriatic plaques include CCL20 (macrophage inflammatory protein 3α, or MIP-3α),58 CCL27 (cutaneous T-cell–attracting chemokine, or CTACK),71 monokine induced by interferon-γ (MIG),73 or RANTES (regulated on activation, normal T-cell expressed and secreted), and monocyte chemotactic protein 1 (MCP-1).
It is thought that neutrophils, another leukocyte population abundantly present in psoriatic infiltrates, are recruited by the neutrophil-attracting chemokine interleukin-8 (CXCL8). However, this pathway is probably not the exclusive means of neutrophil recruitment, since an interleukin-8–blocking monoclonal antibody had only modest efficacy in a clinical study.74
In addition to the mediators involved in leukocyte recruitment and activation, substances such as neuropeptides appear to be involved in the pathogenesis of psoriasis. These include substance P and nerve growth factor, along with its receptor, the p75 neurotrophin receptor, and tyrosine kinase A.75,76 That neuropathogenic mechanisms contribute to the development of psoriasis is further suggested by the increase in terminal cutaneous nerves within psoriatic lesions. Finally, clinical observations, such as the symmetric distribution pattern of psoriatic lesions and the resolution of psoriasis at sites of administration of local anesthesia, are currently interpreted as evidence of the intimate involvement of the nervous system in the pathogenesis of psoriasis.
As in other inflammatory disorders, leukocyte recruitment to psoriatic skin occurs in consecutive steps mediated by complex interactions of cytokines, chemokines, and adhesion receptors.77,78 Although psoriasis-specific steps have not been identified, this disease has served as a model for in-depth investigations of several adhesion-molecule interactions that are of general importance in the generation of inflammatory reactions.41,42
The first step of leukocyte recruitment is the transition from free flow in the vascular lumen to a rolling motion along the endothelium of the vessel wall, mediated primarily by a family of adhesion molecules called selectins.77-80 Activated endothelial cells express P-selectin (CD62P) and E-selectin (CD62E).81 The pivotal role of selectins in leukocyte rolling has been confirmed in many experimental approaches that interfere with their adhesive interactions.81 Selectin functions overlap to a considerable extent, as can be concluded from the efficacy of selectin-blocking strategies. A monoclonal antibody that was specifically directed against E-selectin failed to alleviate psoriasis in a recent clinical trial, whereas less selective compounds, such as efomycine M, which inhibits both E-selectin and P-selectin, showed significant anti-psoriatic efficacy in animal models.82,83
Endothelial cells express E-selectin, which can interact with specific ligands expressed by T cells. These ligands are transmembrane glycoproteins bearing a special carbohydrate moiety, called sialyl-LewisX, displayed on cell-surface proteins.81 T lymphocytes localizing to the skin express the sialyl-LewisX–bearing CLA,84 which is thought to confer the tissue selectivity of these cells, at least in part.85
Once rolling leukocytes are subject to activation by chemokines, they attach firmly to the endothelium through the interactions between β2 integrins (e.g., LFA-1, or αLβ2 integrin) and adhesion molecules of the immunoglobulin superfamily, such as ICAM-1 (CD54). Additional interactions occur between β1 integrins and their ligands, such as α4β1 integrin and vascular-cell adhesion molecule 1. The importance of LFA-1 in T-cell recruitment into the skin is highlighted by the antipsoriatic efficacy of efalizumab, a new monoclonal antibody directed against LFA-1.41,42
In contrast to the relatively well understood process of lymphocyte extravasation, little is known about the subsequent migration through the cutaneous extracellular matrix and the processes determining the ultimate localization and arrest of lymphocytes within the epidermal compartment. The epidermis of psoriatic skin is characterized by induced expression of ICAM-1 (Figure 2E).63,86 ICAM-1, induced by proinflammatory cytokines, enables activated lymphocytes to attach through their surface molecules, such as LFA-1.42 In addition, other adhesion molecules may contribute to epidermal T-cell localization.78 For example, the αE(CD103)β7 integrin (Figure 2G), which binds to epidermal E-cadherin,87 has been implicated in epidermal recruitment of CD8+ T cells in psoriatic lesions.33,88 However, it is also possible that lymphocytes are transported passively to the upper epidermal layers owing to the accelerated upward migration of keratinocytes in psoriasis. Overall, given the central role of T lymphocytes in the pathogenesis of psoriasis, agents that would influence the function or recruitment of leukocytes are appealing therapeutic compounds.89,90
Therapy
Most accepted treatments for psoriasis have been developed empirically or were found by chance. However, recent insights into the immunopathogenesis of psoriasis have further elucidated the mode of action of some accepted compounds91,92 and have provided new treatment strategies.93,94 The severity of the disease usually determines the therapeutic approach. Approximately 70 to 80 percent of all patients with psoriasis can be treated adequately with use of topical therapy. Mainly for practical reasons, the vitamin D3 analogues (calcipotriol and tacalcitol) and the topical retinoid tazarotene — all of which affect keratinocyte functions and the immune response — are in wider use than is either anthralin or coal tar. Since most of the compounds that have been mentioned may irritate delicate areas of skin, topical corticosteroids are used in combination with those compounds, particularly in intertriginous areas.
In cases of moderate-to-severe psoriasis (e.g., affecting large surface areas), the use of phototherapy, systemic drugs, or both must be considered. Among the established regimens, various therapeutic methods may have distinct modes of action. For example, fumarates and cyclosporine are primarily immunosuppressive agents, whereas retinoids and methotrexate also target keratinocyte functions. Rational combination treatments target inflammation as well as epidermal alterations and may provide improved efficacy and safety. Thus, combinations of topical vitamin D3 analogues with phototherapy or systemic retinoids plus psoralen and ultraviolet A phototherapy (RePUVA) are well-established treatment regimens for psoriasis.
Psoriasis in children, in pregnant women, or in patients with the acquired immunodeficiency syndrome may provide considerable therapeutic challenges, arguably best handled by consultation with a specialist. Likewise, severe nail involvement or pustular psoriasis should be the province of the specialist.
Although most established treatment regimens are reasonably effective as short-term therapy for psoriasis, extended disease control is difficult to achieve because the safety profile of most therapeutic agents limits their long-term use.95 Another unmet medical need is for agents that can be applied easily, since application of various currently available agents is difficult and thus compliance may be problematic. More convenient preparations improve adherence to recommended regimens.96 Patients with severe psoriasis often become frustrated with the management of their disease and the perceived ineffectiveness of the therapies prescribed.97 Studies have indicated that the impairment of the quality of life caused by psoriasis equals or even exceeds that due to other major illnesses such as diabetes, rheumatoid arthritis, and cancer.4,98
As already noted, recent advances in psoriasis research have provided a sound platform for the rational design of new biologic agents and biologic-immune-response modifiers that specifically target key mechanisms of the pathogenesis of psoriasis.41 Three of these agents — alefacept, efalizumab, and etanercept — are currently approved by the Food and Drug Administration (FDA) for the treatment of psoriasis; several others (e.g., infliximab) are in the final phase of clinical development. The most promising compounds are monoclonal antibodies, cytokines, and fusion proteins. Three fundamental modes of action are being explored: decreasing the number of pathogenic T cells, blocking T-cell migration and adhesion, and antagonizing effector cytokines (Figure 5Figure 5
New Pathogenesis-Oriented Therapeutic Principles.).As demonstrated by antibody-mediated targeting of CD4 on helper T cells43,44,99 or by targeting of the T-cell–expressed interleukin-2 receptor with an interleukin-2–diphtheria toxin,39 psoriasis can be alleviated by decreasing the number of pathogenic T cells. The first biologic agent approved by the FDA for treating psoriasis was alefacept, a fusion protein in which the binding site of leukocyte-function–associated antigen 3 (LFA-3) and the human IgG Fc portion are combined. Alefacept binds to CD2 on activated T cells, thus impairing costimulatory signals delivered by LFA-3 and (possibly the best explanation for the long-lasting effect in the subgroup of patients who respond to the drug) inducing apoptosis in circulating memory T cells.40
Interruption of the molecular cascade resulting in cutaneous recruitment of pathogenic leukocytes has been achieved by efalizumab, a humanized monoclonal antibody that is directed against an extracellular epitope of the LFA-1 α chain, which was approved by the FDA for the treatment of psoriasis in October 2003.42 Other substances, which include small-molecule compounds, are currently under development.78
A key cytokine in psoriasis (and in other inflammatory diseases) is TNF-α, which can be functionally inhibited by the chimeric antibody infliximab or by the recombinant human TNF-receptor fusion protein etanercept. Both agents competitively inhibit interactions of TNF-α with cell-surface receptors and show convincing efficacy in treating psoriasis.65,66 Shifting the immunologic microenvironment in psoriatic skin, dominated by Th1-type cytokines through substitution of type 2 helper T-cell–type cytokines, such as interleukin-1069 and interleukin-4,70 has been reported as effective in some cases of psoriasis.
Numerous other biologic agents and immune-response modifiers are under development; all of them use at least one of the mechanisms mentioned above.100 As a class, these compounds have the potential to handle some of the unmet medical needs in the treatment of psoriasis.
Supported by a Rudolf Virchow Award and a research grant (Scho 565/5-1) from the Deutsche Forschungsgemeinschaft (to Dr. Schön).
Dr. Schön reports having received lecture fees from Serono and grant support from 3M Pharmaceuticals. Dr. Boehncke reports having received consulting and lecture fees from Serono, Biogen, and Wyeth and lecture fees from Schering AG.
We are indebted to Professor U. Mrowietz (University of Kiel, Kiel, Germany) for helpful discussions and critical proofreading of the manuscript and to Professor C.E.M. Griffiths (University of Manchester, Manchester, United Kingdom) for a helpful suggestion.
Source Information
From the Rudolf Virchow Center, DFG Research Center for Experimental Biomedicine, and the Department of Dermatology, University of Würzburg, Würzburg (M.P.S.); and the Department of Dermatology, University of Frankfurt, Frankfurt (W.-H.B.) — both in Germany.
Address reprint requests to Dr. Schön at the Rudolf Virchow Center, DFG Research Center for Experimental Biomedicine and Department of Dermatology, Julius Maximilians University, Versbacher Str. 9, 97078 Würzburg, Germany, or at michael.schoen@virchow.uni-wuerzburg.de.
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Full Text
- Glossary
Glossary
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CC chemokines:
A subfamily of small chemoattractant peptides that have two N-terminal cysteine residues adjacent to each other.
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Cutaneous lymphocyte-associated antigen (CLA):
A selectin ligand bearing the sialyl-LewisX carbohydrate moiety; expressed preferentially by skin-homing lymphocytes.
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CXC chemokines:
A subgroup of leukocyte-attracting chemokines with a different amino acid between the two N-terminal cysteine residues.
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Intercellular adhesion molecule 1 (ICAM-1):
Also known as CD54, an adhesion molecule of the immunoglobulin superfamily functioning as a counterreceptor for adhesion molecules of the integrin family; expressed on endothelial cells and some activated epithelial cells.
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Interferon-γ:
A cytokine produced primarily by T lymphocytes, characteristic for immune responses dominated by type 1 helper T (Th1) cells, including psoriasis.
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Leukocyte-function–associated antigen (LFA):
CD11a–CD18, a heterodimeric adhesion molecule of the integrin family expressed by lymphocytes; binds to ICAM-1, ICAM-2, and ICAM-3.
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Major-histocompatibility-complex (MHC) molecules:
Surface molecules important for antigen presentation to T lymphocytes.
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PSORS:
Psoriasis-susceptibility locus, one of several genomic sequences associated with psoriasis.
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SCID mice:
Mice with severe combined immunodeficiency due to a spontaneous mutation and lacking functional B and T lymphocytes; used for transplantation and immunologic transfer studies.
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Transforming growth factor α (TGF-α):
A cytokine involved in some tissue alterations in psoriatic skin.
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Vascular cell adhesion molecule 1:
Also known as CD106; a vascular adhesion molecule of the immunoglobulin superfamily, a counterreceptor for the α4β1 integrin.
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Vascular endothelial growth factor (VEGF):
A key regulator of angiogenesis, overexpressed in psoriatic skin.
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- Letters
