Detection of Type VII Collagen Autoantibodies Before the Onset of Bullous Systemic Lupus Erythematosus
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1 Research Case Report/Case Series Detection of Type VII Collagen utoantibodies efore the Onset of ullous Systemic Lupus Erythematosus Daniel. Grabell, M; Loderick. Matthews, MS; Kim. Yancey, MD; enjamin F. Chong, MD, MSCS IMPORTNCE nti type VII collagen autoantibodies are often detectable in patients with bullous systemic lupus erythematosus (SLE). However, the timing of their appearance preceding the onset of disease is unknown to date. OSERVTIONS We report the case of a 50-year-old woman with a history of SLE who was seen with vesicles and bullae around her lips, trunk, axillae, arms, and thighs. Histologic analysis and immunofluorescence and immunoblot studies confirmed the diagnosis of SLE. Immunoblotting and enzyme-linked immunosorbent assay studies of the patient s serum obtained 3 months before the onset of SLE showed the presence of anti type VII collagen autoantibodies. Levels of anti type VII collagen IgG increased after bullous lesions appeared. Within 1 month after initiating dapsone therapy and increasing the dosage of prednisone, skin lesions promptly resolved. One year after the onset of SLE, the anti type VII collagen IgG decreased below levels observed before the inception of the bullous lesions. CONCLUSIONS ND RELEVNCE nti type VII collagen autoantibodies can precede the clinical appearance of SLE. The subsequent increase and decrease in levels of circulating anti type VII collagen autoantibodies, which mirrored skin disease activity, support a potential role in their initiation of disease. JM Dermatol. 2015;151(5): doi: /jamadermatol Published online February 11, uthor ffiliations: Department of Dermatology, University of Texas Southwestern Medical Center, Dallas. Corresponding uthor: enjamin F. Chong, MD, MSCS, Department of Dermatology, University of Texas Southwestern Medical Center, 5323 Harry Hines lvd, Dallas, TX (ben.chong@utsouthwestern.edu). ullous systemic lupus erythematosus (SLE) is a rare vesiculobullous eruption favoring photoexposed areas and mucous membranes. Vesicles and bullae of varying sizes can appear with crusting and resolve as hyperpigmented patches. The absence of milia and scarring, as well as the prominence in trauma-prone areas, distinguishes this entity from epidermolysis bullosa acquisita (E). The histology of SLE primarily shows subepidermal blisters and neutrophilic upper dermal infiltrates; direct immunofluorescence studies of normal-appearing perilesional skin demonstrate immunoglobulin and complement deposition at the basement membrane zone. 1 While other antigenic targets, such as bullous pemphigoid antigen 1, laminin-5, and laminin-6, have been reported in SLE, 2 anti type VII collagen autoantibodies have been detected in the serum of many patients with SLE. 3 s the major component of the anchoring fibrils, type VII collagen links the lamina densa to the underlying dermis. 4 lthough autoantibodies in the serum of patients with SLE before their diagnosis have been previously observed, 5 whether circulating anti type VII collagen autoantibodies are present before the appearance of SLE is unknown. We describe a patient with SLE whose serum contained IgG anti type VII collagen autoantibodies before SLE onset. Moreover, after the SLE resolved, the anti type VII collagen IgG levels diminished below those documented before the onset of the immunobullous disease. Report of a Case 50-year-old frican merican woman with type II diabetes mellitus and a 6-month history of SLE was seen at the University of Texas Southwestern dermatology outpatient clinic. She manifested positive merican College of Rheumatology SLE criteria, 6 including arthritis, oral ulcers, photosensitivity, discoid lupus erythematosus, positive antinuclear antibody test results, and immunologic disorder (positive anti Smith antibodies). She had a 3-week history of a pruritic, vesiculobullous eruption covering her perioral area, trunk, axillae, arms, and inner thighs. t the onset of the eruption, the patient was taking prednisone (7.5 mg daily), which had been tapered from 15 mg daily 1 month previously. She had also been taking chloroquine phosphate (250 mg daily on weekdays and 125 mg daily on weekends) and mycophenolate mofetil (500 mg twice daily) for the past 3 months. In response to the rash and presumed lupus flare due to her arthritis, the elevated double-stranded DN titers, and her low complement levels, her rheumatologist had increased the prednisone dos- jamadermatology.com (Reprinted) JM Dermatology May 2015 Volume 151, Number 5 539
2 Research Case Report/Case Series Type VII Collagen utoantibodies efore SLE Onset Figure 1. ullous Systemic Lupus Erythematosus in an frican merican Woman, Shown are multiple small and large tense vesicles and bullae in the patient s right axilla., Vesicles and bullae with surrounding erythematous plaques with hemorrhagic crusting are seen in the perioral area. age to 30 mg daily. The patient also had discontinued the mycophenolate mofetil and chloroquine herself because she was concerned about drug reactions. On physical examination, multiple tense vesicles and bullae with hemorrhagic crusting and annular erythematous plaques were observed on her back, chest, abdomen, eyebrows, forearms, upper arms, inner thighs, axillae (Figure 1), and perioral area (Figure 1). The patient had diffuse scarring alopecia on her scalp, with hypopigmented patches and underlying erythema on the crown, consistent with discoid lupus erythematosus. biopsy specimen from the edge of a bulla on the right upper arm showed a subepidermal vesiculobullous dermatosis with neutrophils, occasional lymphocytes, and red blood cells within the blister cavity and a sparse perivascular infiltrate with lymphocytes and neutrophils (Figure 2). Direct immunofluorescence showed a linear pattern (Figure 2) of C3, Ig, and IgG along the basement membrane zone. Indirect immunofluorescence studies of the patient s serum on salt-split skin (which is normal skin treated with 1M sodium chloride that splits the epidermis and dermis at the basement membrane level) showed positive IgG binding to the dermal side at a titer of 1:10 (Figure 2C). Immunoblot studies of a recombinant of the noncollagenous (NC1) domain of type VII collagen confirmed that the patient had IgG autoantibodies directed against this signature autoantigen (Figure 3). fter the diagnosis of SLE was made, the patient was treated with dapsone (50 mg twice daily) and commenced a tapering dose of prednisone, starting at 40 mg daily. One month later, the patient had experienced a significant decrease in vesicles. fter 3 months of skin inactivity, the patient s prednisone was discontinued, and dapsone was discontinued 4 months later. Twelve months after the eruption, the patient had hyperpigmented macules and patches in her perioral area, axillae, trunk, and arms, with no bullae or vesicles. Three months before her SLE onset, a serum sample had been collected from the patient, who had been receiving a stable dosage of prednisone (15 mg daily) for 2 months because she had enrolled in the University of Texas Southwestern Cutaneous Lupus Registry, which is a longitudinal observational study of the disease course of patients with cutaneous lupus. Twelve months after her SLE appeared, another serum sample was drawn from the patient, who had been taking chloroquine phosphate (250 mg daily) for 4 months. Immunofluorescence studies of the serum sample drawn before SLE onset on salt-split skin showed IgG bound to the dermal side at a titer of 1:5 (Figure 3). Immunoblot studies of the NC1 type VII collagen recombinant again demonstrated IgG autoantibodies against this particular antigen in the serum samples drawn 3 months before and 3 weeks after the eruption had started (Figure 3). During the course of the patient s immunobullous lesions, quantitation of IgG anti type VII collagen autoantibodies by enzyme-linked immunosorbent assay (ML International) revealed sequential values of 9.23 U/mL (3 months before disease onset), U/mL (3 weeks after disease onset), and 2.30 U/mL (12 months after disease onset). Discussion This case report describes novel findings in a patient with SLE with anti type VII collagen autoantibodies in her serum 3 months before the onset of the disease. fter these autoantibodies had increased 3 weeks following the development of her eruption, resolution of her rash was accompanied by a subsequent decrease in these autoantibodies. Found in the lamina densa and the sublamina densa fibrillar area of the dermal-epidermal junction, type VII collagen is composed of 3 α chains containing a central collagenous triple helix and domains in the amino-terminal (NC1) and carboxy- 540 JM Dermatology May 2015 Volume 151, Number 5 (Reprinted) jamadermatology.com
3 Type VII Collagen utoantibodies efore SLE Onset Case Report/Case Series Research Figure 2. Pathology Studies Supporting the ullous Systemic Lupus Erythematosus Diagnosis C, Histologic analysis of a biopsy specimen from the right upper arm shows a subepidermal bulla with separation of the epidermis from the underlying dermis., Direct immunofluorescence study shows IgG with a strong linear deposition along the basement membrane zone. C, Indirect immunofluorescence study of serum obtained from the patient during her active disease flare shows IgG at a 1:10 titer binding to the dermal side of 1M salt-split skin. Original magnification 200. Figure 3. nti Type VII Collagen utoantibodies efore, During, and fter the Onset of ullous Systemic Lupus Erythematosus terminal (NC2) ends. 7 The immunodominant domains of type VII collagen recognized by IgG autoantibodies from patients with, Immunoblot study on a recombinant of the NC1 domain of type VII collagen shows IgG binding to the signature autoantigen (arrow). Lane 1 shows normal control serum. Lane 2 shows the serum of a patient with epidermolysis bullosa acquisita. The serum of the case patient at 1:40 dilution is shown 3 months before eruption (lane 3) and 3 weeks after rash onset (lane 4)., Indirect immunofluorescence study of the case patient s serum 3 months before disease onset shows IgG binding to the dermal side of the dermal-epidermal junction in salt-split skin at a 1:5 titer (original magnification 200). SLE (and E) reside in the NC1 domain. 3,8 Passive transfer of purified rabbit anti type VII collagen IgG in adult nude, alb/c, jamadermatology.com (Reprinted) JM Dermatology May 2015 Volume 151, Number 5 541
4 Research Case Report/Case Series Type VII Collagen utoantibodies efore SLE Onset Table. nti Type VII Collagen IgG Levels in the Serum Samples of the Case Patient 3 Months efore, 3 Weeks fter, and 12 Months fter Disease Onset and in Other Patients and Healthy Control Subjects nti Type VII Collagen Sample IgG Level, U/mL Case patient with bullous systemic lupus erythematosus 3 mo efore disease onset wk fter disease onset mo fter disease onset 2.30 Other patients, mean (SD) Patients with epidermolysis bullosa (67.01) acquisita (n = 2) Healthy control subjects (n = 14) a 0.11 (0.40) Patients with discoid lupus 0.36 (0.93) erythematosus (n = 13) a Patients with systemic lupus 0.23 (0.37) erythematosus (n = 13) a a Serum samples were obtained from the University of Texas Southwestern Cutaneous Lupus Registry and showed significantly lower anti type VII collagen IgG levels compared with patients with epidermolysis bullosa acquisita (P <.01). None of the samples were positive for anti type VII collagen IgG. and C57L/6 mice resulted in the formation of skin blisters and erosions. 9 Similarly, purified anti type VII collagen antibodies from the serum of patients with E injected in hairless mice showed that these antibodies can induce E-like skin lesions. 10 ased on our observations that anti type VII collagen autoantibodies had been present in our patient before and had increased after her bullous lesions appeared, we hypothesize that there is a critical threshold of these antibodies in circulation that is surpassed before the skin eruption occurs in SLE. The presence and accumulation of circulating autoantibodies have been previously observed in patients with lupus. large prospective study 5 of 130 military recruits who were followed up before their SLE diagnosis showed that multiple autoantibodies, such as antinuclear antibodies and anti doublestranded DN antibodies, were present in their blood years before their diagnosis and the onset of systemic symptoms. Moreover, 58% of patients with SLE showed escalating doublestranded DN antibody levels leading up to their SLE diagnosis. 11 case for the pathogenic potential of autoantibodies in lupus can be made with neonatal lupus, in which transplacental transfer of Ro, La, and ribonucleoprotein autoantibodies occurs from mother to fetus. 12 The disease wanes as these autoantibodies level off or decline. 13 Moreover, patients with Sjögren s syndrome with positive Ro autoantibodies have been observed to later develop subacute cutaneous lupus. 14 Using the serum sample repository from the University of Texas Southwestern Cutaneous Lupus Registry, we also measured anti type VII collagen IgG by enzyme-linked immunosorbent assay in age and sex matched patients with SLE (n = 13), patients with discoid lupus erythematosus (n = 13), and healthy control subjects (n = 14). ll these serum samples had levels of anti type VII collagen IgG below the established positive threshold. The same samples were lower than those observed in our patient s serum before and during the SLE eruption and in the serum samples from 2 patients with E serving as positive controls (Table). We were able to confirm findings from a previous study 15 that the serum of patients with SLE without SLE does not contain significant levels of anti type VII collagen autoantibodies. Twelve months after the initial eruption, our patient s serum showed markedly decreased levels of anti type VII collagen IgG. t that time, the patient s SLE was quiescent. similar finding was previously reported in a patient with Sjögren s syndrome and SLE overlap with SLE, whose anti type VII collagen IgG was undetectable at the time of SLE remission. 16 The rise and fall in levels of anti type VII collagen autoantibodies during the course of a patient s SLE disease imply that they have possible usefulness as biomarkers, which can be used to assess disease activity and guide treatment. Limitations of this study include the small sample size (with the findings observed in 1 patient) and the limited follow-up period of 1 year. In addition, the use of concurrent immunosuppressant medications may alter autoantibody levels. However, the patient herein was receiving stable dosages of her immunosuppressants before and after her SLE eruption. Conclusions In summary, anti type VII collagen autoantibodies were detected 3 months before the inception of SLE in a patient with SLE. Their levels subsequently increased after disease onset and decreased with disease resolution. We hypothesize that surpassing a critical level of anti type VII collagen autoantibodies may be an important event in the evolution of SLE. n alternative explanation would be that the patient had nonpathogenic autoantibodies before her SLE. Epitope spreading may be responsible for the appearance of pathogenic autoantibodies, resulting in epidermal-dermal separation and eventual onset of her SLE. 2,17 Larger prospective studies in patients with SLE measuring levels of anti type VII collagen autoantibodies throughout their disease course for an extended time frame would be helpful in determining whether these autoantibodies could be reliable disease markers. RTICLE INFORMTION ccepted for Publication: October 15, Published Online: February 11, doi: /jamadermatol uthor Contributions: Mr Grabell and Dr Chong had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Grabell, Yancey, Chong. cquisition, analysis, or interpretation of data: ll authors. Drafting of the manuscript: Grabell, Chong. Critical revision of the manuscript for important intellectual content: ll authors. Statistical analysis: Grabell, Chong. Obtained funding: Yancey, Chong. dministrative, technical, or material support: Matthews, Yancey, Chong. Study supervision: Chong. Conflict of Interest Disclosures: Dr Chong reported being an investigator for Daavlin Corporation. Dr Yancey reported serving on advisory boards for Stiefel/GlaxoSmithKline and Mary Kay, Inc. No other disclosures were reported. Funding/Support: This study was supported in part by grant K23R from the National Institute of rthritis and Musculoskeletal and Skin Diseases, National Institutes of Health. 542 JM Dermatology May 2015 Volume 151, Number 5 (Reprinted) jamadermatology.com
5 Dermatology Over the Rainbow Case Report/Case Series Research Role of the Funder/Sponsor: The funding source had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the University of Texas Southwestern Medical Center and its affiliated academic and health care centers, the National Center for Research Resources, and the National Institutes of Health. dditional Contributions: Rose Cannon (Department of Dermatology, University of Texas Southwestern Medical Center) provided administrative support in the preparation of the manuscript. REFERENCES 1. Sebaratnam DF, Murrell DF. ullous systemic lupus erythematosus. Dermatol Clin. 2011;29(4): Chan LS, Lapiere JC, Chen M, et al. ullous systemic lupus erythematosus with autoantibodies recognizing multiple skin basement membrane components, bullous pemphigoid antigen 1, laminin-5, laminin-6, and type VII collagen. rch Dermatol. 1999;135(5): Gammon WR, Murrell DF, Jenison MW, et al. utoantibodies to type VII collagen recognize epitopes in a fibronectin-like region of the noncollagenous (NC1) domain. J Invest Dermatol. 1993;100(5): Morris NP, Keene DR, Glanville RW, entz H, urgeson RE. The tissue form of type VII collagen is an antiparallel dimer. J iol Chem. 1986;261(12): rbuckle MR, McClain MT, Rubertone MV, et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349(16): Tan EM, Cohen S, Fries JF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. rthritis Rheum. 1982;25(11): Parente MG, Chung LC, Ryynänen J, et al. Human type VII collagen: cdn cloning and chromosomal mapping of the gene. Proc Natl cad SciUS. 1991; 88(16): Lapiere JC, Woodley DT, Parente MG, et al. Epitope mapping of type VII collagen: identification of discrete peptide sequences recognized by sera from patients with acquired epidermolysis bullosa. J Clin Invest. 1993;92(4): Sitaru C, Mihai S, Otto C, et al. Induction of dermal-epidermal separation in mice by passive transfer of antibodies specific to type VII collagen. J Clin Invest. 2005;115(4): Woodley DT, Ram R, Doostan, et al. Induction of epidermolysis bullosa acquisita in mice by passive transfer of autoantibodies from patients. J Invest Dermatol. 2006;126(6): rbuckle MR, James J, Kohlhase KF, Rubertone MV, Dennis GJ, Harley J. Development of anti-dsdn autoantibodies prior to clinical diagnosis of systemic lupus erythematosus. Scand J Immunol. 2001;54(1-2): Lee L. Transient autoimmunity related to maternal autoantibodies: neonatal lupus. utoimmun Rev. 2005;4(4): Lee L. Cutaneous lupus in infancy and childhood.lupus. 2010;19(9): Provost TT, Talal N, Harley J, Reichlin M, lexander E. The relationship between anti-ro (SS-) antibody positive Sjögren s syndrome and anti-ro (SS-) antibody positive lupus erythematosus. rch Dermatol. 1988;124(1): Ishikawa O, Zaw KK, Miyachi Y, Hashimoto T, Tanaka T. The presence of anti basement membrane zone antibodies in the sera of patients with non-bullous lupus erythematosus. r J Dermatol. 1997;136(2): Fujii K, Fujimoto W, Ueda M, Makino E, rata J. Detection of anti type VII collagen antibody in Sjögren s syndrome/lupus erythematosus overlap syndrome with transient bullous systemic lupus erythematosus. r J Dermatol. 1998;139(2): Noe MH, Chen M, Woodley DT, Fairley J. Familial epidermolysis bullosa acquisita. Dermatol Online J. 2008;14(12):2. NOTLE NOTES Dermatology Over the Rainbow Deshan F. Sebaratnam, MS(Hons); Rashi Minocha, MS; Pablo Fernández-Peñas, PhD When devising morphological descriptions, it would seem that dermatologists in years gone by had their heads in the clouds, with several descriptions alluding to phenomena related to the weather. During the uerger test, the reactive hyperemia observed in patientswithperipheralvasculardiseaseisoftendescribedasa sunsetred. The vesicles of cutaneous anthrax are often described as cloudy, as is the saliva of patients with Sjögren disease. Miliaria crystallina have been likened to dew drops, and the classical description of varicella zoster is thatof dewdropsonrosepetals. Thedistributionandmorphologiccharacteristics of guttate psoriasis have been likened to raindrops, and the dyschromia of chronic arsenic toxicity has been more vividly compared to rain drops on a dusty road. Dermoscopic examination of Kaposi sarcomas may sometimes reveal a multicolored rainbow, 1 livedo racemosa has been compared to bolts of lightning, and perhaps one of the most fascinating clinical signs in dermatology is the Lichtenberg figures that appear on patients who have been struck by lightning. Winter brings with it a range of descriptions such as the footprints in the snow of pseudopelade. 2 Snowflake opacities are seen in the cornea of patients with onchocerciasis, and frosting is a clinical end point often sought in chemical peels. In dermatology, an erosion refers to a loss of epidermis, although erosion also refers to weathering of soil, rocks, and other geologic structure by the action of nature. The night sky has further inspired a range of descriptions. The lunula derives its name from its crescent shape, which resembles that of a halfmoon. Several lesions are described as having stellate morphologic characteristics, includingkeratosislichenoideschronica, atrophieblanche, calciphylaxis,andthecentralwhitepatchesofdermatofibromas.thestarbust pattern is observed in Spitz nevi, and the red comet sign is observed in the nail beds of patients with tuberous sclerosis. Histopathologically, precursor lymphoblastic lymphoma is said to resemble a starry sky, and patients with argyria are reported to have silver deposits forming a stars in heaven pattern under dark-field examination The celestial realm has informed countless descriptions in dermatology. While the connections at times may seem tenuous, the silver lining is that they aid recall and brighten one s day. uthor ffiliations: Department of Dermatology, Westmead Hospital, Westmead, New South Wales, ustralia. Corresponding uthor: Rashi Minocha, MS, Department of Dermatology, Westmead Hospital, Hawkesbury Road, Wentworthville, NSW 2145, ustralia (rashiminocha@live.com.au). Published Online: February 11, doi: /jamadermatol Satta R, Fresi L, Cottoni F. Dermoscopic rainbow pattern in Kaposi s sarcoma lesions: our experience.rch Dermatol. 2012;148(10): Sullivan JR, Kossard S. cquired scalp alopecia, part I: a review. ustralas J Dermatol. 1998;39(4): jamadermatology.com (Reprinted) JM Dermatology May 2015 Volume 151, Number 5 543
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