Pemphigus Vulgaris Autoantibody Profiling by Proteomic Technique

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Kalantari Dehaghi, Mina ^a   Anhalt, Grant J ^b   Camilleri, Michael J ^c   Chernyavsky, Alex I ^a   Chun, Sookhee ^a   Felgner, Philip L ^a   Jasinskas, Algis ^a   Leiferman, Kristin M ^d   Liang, Li ^a   Marchenko, Steve ^a   Nakajima Sasaki, Rie ^a   Pittelkow, Mark R ^c   Zone, John J ^d   Grando, Sergei A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c MAYO CLINIC   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CD1B ANTIGEN; CD32 ANTIGEN; CD33 ANTIGEN; CELL ADHESION MOLECULE; CELL ANTIGEN; CHOLINERGIC RECEPTOR; COMPLEMENT COMPONENT C5A RECEPTOR; DSC1 ANTIGEN; DSC3 ANTIGEN; HLA DR ANTIGEN; HLA E ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOCHONDRIAL PROTEIN; PERIPHERAL MYELIN PROTEIN 22; PKP3 ANTIGEN; PROTEIN CHRM3; PROTEIN CHRNE; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ANXA8L1 GENE; ARTICLE; ATP2C1 GENE; AUTOIMMUNITY; CD1B GENE; CD32 GENE; CD33 GENE; CD88 GENE; CDH8 GENE; CDH9 GENE; CHRM3 GENE; CHRND GENE; CHRNE GENE; COL21A1 GENE; CONTROLLED STUDY; CYB5B GENE; DISEASE SEVERITY; DSC1 GENE; DSC3 GENE; FH GENE; GENE; GP1BA GENE; HLA E GENE; HUMAN; KERATINOCYTE; MAJOR CLINICAL STUDY; MICROARRAY ANALYSIS; MOLECULAR MODEL; NDUFS1 GENE; PDHA1 GENE; PEMPHIGUS VULGARIS; PKP3 GENE; PMP22 GENE; PROTEIN MICROARRAY; PROTEOMICS; SENSITIVITY ANALYSIS; SLC36A4 GENE; SOD2 GENE;

ANTIBODY SPECIFICITY; AUTOANTIBODIES; AUTOANTIGENS; DESMOGLEIN 3; HUMANS; PEMPHIGUS; PRINCIPAL COMPONENT ANALYSIS; PROTEIN ARRAY ANALYSIS; PROTEOMICS; SENSITIVITY AND SPECIFICITY;

EID: 84874749173     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057587     Document Type: Article

References (99)

1. Beutner EH, Lever WF, Witebsky E, Jordon R, Chertock B, (1965) Autoantibodies in Pemphigus Vulgaris: Response to an Intercellular Substance of Epidermis. JAMA 192: 682-688.
2. Anderson HJ, Newcomer VD, Landau JW, Rosenthal LH, (1970) Pemphigus and other diseases. Results of indirect intercellular immunofluorescence. Arch Dermatol 101: 538-546.
3. Pisanti S, Sharav Y, Kaufman E, Posner LN, (1974) Pemphigus vulgaris: incidence in Jews of different ethnic groups, according to age, sex, and initial lesion. Oral Surg Oral Med Oral Pathol 38: 382-387.
4. Chams-Davatchi C, Valikhani M, Daneshpazhooh M, Esmaili N, Balighi K, et al. (2005) Pemphigus: analysis of 1209 cases. International Journal of Dermatology 44: 470-476.
5. Carson PJ, Hameed A, Ahmed AR, (1996) Influence of treatment on the clinical course of pemphigus vulgaris. Journal of the American Academy of Dermatology 34: 645-652.
6. Ahmed AR, Moy R, (1982) Death in pemphigus. Journal of the American Academy of Dermatology 7: 221-228.
7. Rosenberg FR, Sanders S, Nelson CT, (1976) Pemphigus: a 20-year review of 107 patients treated with corticosteroids. Archives of Dermatology 112: 962-970.
8. Amagai M, Stanley JR, (2012) Desmoglein as a target in skin disease and beyond. J Invest Dermatol 132: 776-784.
9. Lambert LL, Spriet E, Vandewiele A, Naeyaert J, (2006) Desmoglein 1 and 3 IgG auto-antibody titers do not correlate with pemphigus disease activity in a prospective study. J Invest Dermatol 126 (Suppl. 1): 11 (Abstract 65).
10. Abasq C, Mouquet H, Gilbert D, Tron F, Grassi V, et al. (2009) ELISA testing of anti-desmoglein 1 and 3 antibodies in the management of pemphigus. Arch Dermatol 145: 529-535.
11. Kamiya K, Aoyama Y, Shirafuji Y, Hamada T, Morizane S, et al. (2012) Detection of antibodies against the non-calcium-dependent epitopes of desmoglein 3 in pemphigus vulgaris and their pathogenic significance. British Journal of Dermatology 167: 252-261.
12. Akman A, Uzun S, Alpsoy E, (2010) Immunopathologic features of pemphigus in the east Mediterranean region of Turkey: a prospective study. Skinmed 8: 12-16.
13. Arin MJ, Engert A, Krieg T, Hunzelmann N, (2005) Anti-CD20 monoclonal antibody (rituximab) in the treatment of pemphigus. Br J Dermatol 153: 620-625.
14. Kwon EJ, Yamagami J, Nishikawa T, Amagai M, (2008) Anti-desmoglein IgG autoantibodies in patients with pemphigus in remission. J Eur Acad Dermatol Venereol 22: 1070-1075.
15. Sharma VK, Prasad HR, Khandpur S, Kumar A, (2006) Evaluation of desmoglein enzyme-linked immunosorbent assay (ELISA) in Indian patients with pemphigus vulgaris. Int J Dermatol 45: 518-522.
16. Belloni-Fortina A, Faggion D, Pigozzi B, Peserico A, Bordignon M, et al. (2009) Detection of autoantibodies against recombinant desmoglein 1 and 3 molecules in patients with pemphigus vulgaris: correlation with disease extent at the time of diagnosis and during follow-up. Clin Dev Immunol 2009: 187864.
17. Khandpur S, Sharma VK, Sharma A, Pathria G, Satyam A, (2010) Comparison of enzyme-linked immunosorbent assay test with immunoblot assay in the diagnosis of pemphigus in Indian patients. Indian J Dermatol Venereol Leprol 76: 27-32.
18. Horvath B, Huizinga J, Pas HH, Mulder AB, Jonkman MF, (2012) Low-dose rituximab is effective in pemphigus. British Journal of Dermatology 166: 405-412.
19. Brandsen R, Frusic-Zlotkin M, Lyubimov H, Yunes F, Michel B, et al. (1997) Circulating pemphigus IgG in families of patients with pemphigus: comparison of indirect immunofluorescence, direct immunofluorescence, and immunoblotting. Journal of the American Academy of Dermatology 36: 44-52.
20. Kricheli D, David M, Frusic-Zlotkin M, Goldsmith D, Rabinov M, et al. (2000) The distribution of pemphigus vulgaris-IgG subclasses and their reactivity with desmoglein 3 and 1 in pemphigus patients and their first-degree relatives. Br J Dermatol 143: 337-342.
21. Torzecka JD, Narbutt J, Sysa-Jedrzejowska A, Waszczykowska E, Lukamowicz J, et al. (2003) Detection of pemphigus autoantibodies by IIF and ELISA tests in patients with pemphigus vulgaris and foliaceus and in healthy relatives. Med Sci Monit 9: CR528-533.
22. Torzecka JD, Wozniak K, Kowalewski C, Waszczykowska E, Sysa-Jedrzejowska A, et al. (2007) Circulating pemphigus autoantibodies in healthy relatives of pemphigus patients: coincidental phenomenon with a risk of disease development? Archives for Dermatological Research Archiv fur Dermatologische Forschung 299: 239-243.
23. Hilario-Vargas J, Dasher DA, Li N, Aoki V, Hans-Filho G, et al. (2006) Prevalence of anti-desmoglein-3 antibodies in endemic regions of Fogo Selvagem in Brazil. J Invest Dermatol 126: 2044-2048.
24. Yoshimura T, Seishima M, Nakashima K, Yasuhara Y, Adachi S, et al. (2001) Increased antibody levels to desmogleins 1 and 3 after administration of carbamazepine. Clin Exp Dermatol 26: 441-445.
25. Gallo R, Massone C, Parodi A, Guarrera M, (2002) Allergic contact dermatitis from thiurams with pemphigus-like autoantibodies. Contact Dermatitis 46: 364-365.
26. Cozzani E, Rosa GM, Drosera M, Intra C, Barsotti A, et al. (2010) ACE inhibitors can induce circulating antibodies directed to antigens of the superficial epidermal cells. Archives for Dermatological Research Archiv fur Dermatologische Forschung.
27. Zagorodniuk I, Weltfriend S, Shtruminger L, Sprecher E, Kogan O, et al. (2005) A comparison of anti-desmoglein antibodies and indirect immunofluorescence in the serodiagnosis of pemphigus vulgaris. Int J Dermatol 44: 541-544.
28. Nguyen VT, Lee TX, Ndoye A, Shultz LD, Pittelkow MR, et al. (1998) The pathophysiological significance of non-desmoglein targets of pemphigus autoimmunity. Pemphigus vulgaris and foliaceus patients develop antibodies against keratinocyte cholinergic receptors. Archives of Dermatology 134: 971-980.
29. Di Zenzo G (2012) Pemphigus autoantibodies generated through somatic mutations target the desmoglein-3 cis-interface. J Clin Invest doi:101172/JCI64413.
30. Sherer Y, Gorstein A, Fritzler MJ, Shoenfeld Y, (2004) Autoantibody explosion in systemic lupus erythematosus: more than 100 different antibodies found in SLE patients. Semin Arthritis Rheum 34: 501-537.
31. Hueber W, Robinson WH, (2006) Proteomic biomarkers for autoimmune disease. Proteomics 6: 4100-4105.
32. Tozzoli R, (2008) The diagnostic role of autoantibodies in the prediction of organ-specific autoimmune diseases. Clin Chem Lab Med 46: 577-587.
33. Robinson WH, DiGennaro C, Hueber W, Haab BB, Kamachi M, et al. (2002) Autoantigen microarrays for multiplex characterization of autoantibody responses. Nat Med 8: 295-301.
34. Hueber W, Utz PJ, Steinman L, Robinson WH, (2002) Autoantibody profiling for the study and treatment of autoimmune disease. Arthritis Res 4: 290-295.
35. Plebani M, Pittoni M, Celadin M, Bernardi D, Mion MM, (2009) Recent advances in diagnostic technologies for autoimmune diseases. Autoimmun Rev 8: 238-243.
36. Fathman CG, Soares L, Chan SM, Utz PJ, (2005) An array of possibilities for the study of autoimmunity. Nature 435: 605-611.
37. Kalantari-Dehaghi M, Molina DM, Farhadieh M, John Morrow W, Liang X, et al. (2011) New targets of pemphigus vulgaris antibodies identified by protein array technology. Experimental Dermatology 20: 154-156.
38. Sinha AA, (2012) Constructing immunoprofiles to deconstruct disease complexity in pemphigus. Autoimmunity 45: 36-43.
39. Grando SA, (2000) Autoimmunity to keratinocyte acetylcholine receptors in pemphigus. Dermatology (Basel) 201: 290-295.
40. Davies DH, Liang X, Hernandez JE, Randall A, Hirst S, et al. (2005) Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc Natl Acad Sci U S A 102: 547-552.
41. Luevano M, Bernard HU, Barrera-Saldana HA, Trevino V, Garcia-Carranca A, et al. (2010) High-throughput profiling of the humoral immune responses against thirteen human papillomavirus types by proteome microarrays. Virology.
42. Liang L, Tan X, Juarez S, Villaverde H, Pablo J, et al. (2011) Systems biology approach predicts antibody signature associated with Brucella melitensis infection in humans. J Proteome Res 10: 4813-4824.
43. Amagai M, Karpati S, Prussick R, Klaus-Kovtun V, Stanley JR, (1992) Autoantibodies against the amino-terminal cadherin-like binding domain of pemphigus vulgaris antigen are pathogenic. Journal of Clinical Investigation 90: 919-926.
44. Judd KP, Mescon H, (1979) Comparison of different epithelial substrates useful for indirect immunofluorescence testing of sera from patients with active pemphigus. Journal of Investigative Dermatology 72: 314-316.
45. Jiao D, Bystryn JC, (1997) Sensitivity of indirect immunofluorescence, substrate specificity, and immunoblotting in the diagnosis of pemphigus. J Am Acad Dermatol 37: 211-216.
46. Vigil A, Davies DH, Felgner PL, (2010) Defining the humoral immune response to infectious agents using high-density protein microarrays. Future Microbiology 5: 241-251.
47. Payne AS, Ishii K, Kacir S, Lin C, Li H, et al. (2005) Genetic and functional characterization of human pemphigus vulgaris monoclonal autoantibodies isolated by phage display. J Clin Invest 115: 888-899.
48. Yamagami J, Takahashi H, Ota T, Amagai M, (2008) Genetic characterization of human Dsg3-specific B cells isolated by flow cytometry from the peripheral blood of patients with pemphigus vulgaris. J Dermatol Sci 52: 98-107.
49. Grando SA, (2012) Pemphigus autoimmunity: hypotheses and realities. Autoimmunity 45: 7-35.
50. Amagai M, Hashimoto T, Shimizu N, Nishikawa T, (1994) Absorption of pathogenic autoantibodies by the extracellular domain of pemphigus vulgaris antigen (Dsg3) produced by baculovirus. Journal of Clinical Investigation 94: 59-67.
51. Amagai M, Ishii K, Hashimoto T, Gamou S, Shimizu N, et al. (1995) Conformational epitopes of pemphigus antigens (Dsg1 and Dsg3) are calcium dependent and glycosylation independent. Journal of Investigative Dermatology 105: 243-247.
52. Amagai M, Ishii K, Takayanagi A, Nishikawa T, Shimizu N, (1996) Transport to endoplasmic reticulum by signal peptide, but not proteolytic processing, is required for formation of conformational epitopes of pemphigus vulgaris antigen (Dsg3). Journal of Investigative Dermatology 107: 539-542.
53. Amagai M, Hashimoto T, Green KJ, Shimizu N, Nishikawa T, (1995) Antigen-specific immunoadsorption of pathogenic autoantibodies in pemphigus foliaceus. Journal of Investigative Dermatology 104: 895-901.
54. Amagai M, Nishikawa T, Nousari HC, Anhalt GJ, Hashimoto T, (1998) Antibodies against desmoglein 3 (pemphigus vulgaris antigen) are present in sera from patients with paraneoplastic pemphigus and cause acantholysis in vivo in neonatal mice. Journal of Clinical Investigation 102: 775-782.
55. Dmochowski M, Hashimoto T, Garrod DR, Nishikawa T, (1993) Desmocollins I and II are recognized by certain sera from patients with various types of pemphigus particularly Brazilian pemphigus foliaceus. Journal of Investigative Dermatology 100: 380-384.
56. Dmochowski M, Hashimoto T, Chidgey MAJ, Yue KKM, Wilkinson RW, et al. (1995) Demonstration of antibodies to bovine desmocollin isoforms in certain pemphigus sera. British Journal of Dermatology 133: 519-525.
57. Evangelista F, Dasher DA, Diaz LA, Prisayanh PS, Li N, (2008) E-cadherin is an additional immunological target for pemphigus autoantibodies. J Invest Dermatol 128: 1710-1718.
58. Flores G, Culton DA, Prisayanh P, Qaqish BF, James K, et al. (2012) IgG Autoantibody Response against Keratinocyte Cadherins in Endemic Pemphigus Foliaceus (Fogo Selvagem). J Invest Dermatol.
59. Chen J, Den Z, Koch PJ, (2008) Loss of desmocollin 3 in mice leads to epidermal blistering. Journal of Cell Science 121: 2844-2849.
60. Mao X, Nagler AR, Farber SA, Choi EJ, Jackson LH, et al. (2010) Autoimmunity to desmocollin 3 in pemphigus vulgaris. American Journal of Pathology 177: 2724-2730.
61. Spindler V, Heupel WM, Efthymiadis A, Schmidt E, Eming R, et al. (2009) Desmocollin 3-mediated binding is crucial for keratinocyte cohesion and is impaired in pemphigus. Journal of Biological Chemistry 284: 30556-30564.
62. Amagai M, Ahmed AR, Kitajima Y, Bystryn JC, Milner Y, et al. (2006) Are desmoglein autoantibodies essential for the immunopathogenesis of pemphigus vulgaris, or just 'witnesses of disease'? Exp Dermatol 15: 815-831.
63. Chernyavsky AI, Arredondo J, Piser T, Karlsson E, Grando SA, (2008) Differential coupling of M1 muscarinic and α7 nicotinic receptors to inhibition of pemphigus acantholysis. J Biol Chem 283: 3401-3408.
64. Nguyen VT, Ndoye A, Grando SA, (2000) Novel human α9 acetylcholine receptor regulating keratinocyte adhesion is targeted by pemphigus vulgaris autoimmunity. Am J Pathol 157: 1377-1391.
65. Nguyen VT, Arredondo J, Chernyavsky AI, Pittelkow MR, Kitajima Y, et al. (2004) Pemphigus vulgaris acantholysis ameliorated by cholinergic agonists. Arch Dermatol 140: 327-334.
66. Tirado-Sanchez A, Vazquez-Gonzalez D, Ponce-Olivera RM, Lopez-Lozano HE, (2012) Acetylcholine receptor antibodies in patients with pemphigus vulgaris: correlation with disease extent at the time of diagnosis and during follow-up. Dermatol Online J 18: 14.
67. Botelho-Nogueira L, Quarantini L, Miranda-Scippa A, (2011) Use of anticholinergic drugs and worsening of pemphigus foliaceus in a patient with bipolar disorder. Rev Bras Psiquiatr 33: 412-413.
68. Bastian BC, Nuss B, Romisch J, Kraus M, Brocker EB, (1994) Autoantibodies to annexins: a diagnostic marker for cutaneous disorders? Journal of Dermatological Science 8: 194-202.
69. Nguyen VT, Ndoye A, Grando SA, (2000) Pemphigus vulgaris antibody identifies pemphaxin-a novel keratinocyte annexin-like molecule binding acetylcholine. J Biol Chem 275: 29466-29476.
70. Runkel F, Michels M, Franken S, Franz T, (2006) Specific expression of annexin A8 in adult murine stratified epithelia. J Mol Histol 37: 353-359.
71. Goebeler V, Poeter M, Zeuschner D, Gerke V, Rescher U, (2008) Annexin A8 regulates late endosome organization and function. Molecular Biology of the Cell 19: 5267-5278.
72. Zimmerman UJ, Hennigan BB, Liu L, Campbell CH, Fisher AB, (1995) Annexins I, II and III are specific choline binding proteins. Biochemistry and Molecular Biology International 35: 307-315.
73. Geoghegan W, Jordon R (1992) Anti-mitochondrial IgG1 subclass antibodies in pemphigus foliaceus. Journal of Investigative Dermatology 98: 589, Abstr. #225.
74. Marchenko S, Chernyavsky AI, Arredondo J, Gindi V, Grando SA, (2010) Antimitochondrial autoantibodies in pemphigus vulgaris: a missing link in disease pathophysiology. J Biol Chem 285: 3695-3704.
75. Yesilova Y, Ucmak D, Selek S, Dertlioglu SB, Sula B, et al. (2012) Oxidative stress index may play a key role in patients with pemphigus vulgaris. J Eur Acad Dermatol Venereol.
76. Naziroglu M, Kokcam I, Simsek H, Karakilcik AZ, (2003) Lipid peroxidation and antioxidants in plasma and red blood cells from patients with pemphigus vulgaris. J Basic Clin Physiol Pharmacol 14: 31-42.
77. Yazdanpanah MJ, Ghayour-Mobarhan M, Taji A, Javidi Z, Pezeshkpoor F, et al. (2011) Serum zinc and copper status in Iranian patients with pemphigus vulgaris. International Journal of Dermatology 50: 1343-1346.
78. Arredondo J, Chernyavsky AI, Karaouni A, Grando SA, (2005) Novel mechanisms of target cell death and survival and of therapeutic action of IVIg in pemphigus. Am J Pathol 167: 1531-1544.
79. Gil MP, Modol T, Espana A, Lopez-Zabalza MJ, (2012) Inhibition of FAK prevents blister formation in the neonatal mouse model of pemphigus vulgaris. Experimental Dermatology 21: 254-259.
80. Rainteau D, Mansuelle P, Rochat H, Weinman S, (1995) Characterization and ultrastructural localization of annexin VI from mitochondria. FEBS Lett 360: 80-84.
81. Tigalonowa M, Bjerke JR, Livden JK, Matre R, (1990) The distribution of Fc gamma RI, Fc gamma RII and Fc gamma R III on Langerhans' cells and keratinocytes in normal skin. Acta Derm Venereol 70: 385-390.
82. Lim PL, Zouali M, (2006) Pathogenic autoantibodies: emerging insights into tissue injury. Immunol Lett 103: 17-26.
83. Ihrie RA, Marques MR, Nguyen BT, Horner JS, Papazoglu C, et al. (2005) Perp is a p63-regulated gene essential for epithelial integrity. Cell 120: 843-856.
84. Davies L, Gray D, Spiller D, White MR, Damato B, et al. (2009) P53 apoptosis mediator PERP: localization, function and caspase activation in uveal melanoma. J Cell Mol Med 13: 1995-2007.
85. Hu Z, Bonifas JM, Beech J, Bench G, Shigihara T, et al. (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat Genet 24: 61-65.
86. Sudbrak R, Brown J, Dobson-Stone C, Carter S, Ramser J, et al. (2000) Hailey-Hailey disease is caused by mutations in ATP2C1 encoding a novel Ca(2+) pump. Hum Mol Genet 9: 1131-1140.
87. Behne MJ, Tu CL, Aronchik I, Epstein E, Bench G, et al. (2003) Human keratinocyte ATP2C1 localizes to the Golgi and controls Golgi Ca2+ stores. J Invest Dermatol 121: 688-694.
88. Seishima M, Esaki C, Osada K, Mori S, Hashimoto T, et al. (1995) Pemphigus IgG, but not bullous pemphigoid IgG, causes a transient increase in intracellular calcium and inositol 1,4,5-triphosphate in DJM-1 cells, a squamous cell carcinoma line. Journal of Investigative Dermatology 104: 33-37.
89. Kitajima Y, (2002) Mechanisms of desmosome assembly and disassembly. Clin Exp Dermatol 27: 684-690.
90. Ware J, Russell S, Ruggeri ZM, (1997) Cloning of the murine platelet glycoprotein Ibalpha gene highlighting species-specific platelet adhesion. Blood Cells Mol Dis 23: 292-301.
91. Taylor VC, Buckley CD, Douglas M, Cody AJ, Simmons DL, et al. (1999) The myeloid-specific sialic acid-binding receptor, CD33, associates with the protein-tyrosine phosphatases, SHP-1 and SHP-2. Journal of Biological Chemistry 274: 11505-11512.
92. Gerard C, Gerard NP, (1994) C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu Rev Immunol 12: 775-808.
93. Jordon RE, Kawana S, Fritz KA, (1985) Immunopathologic mechanisms in pemphigus and bullous pemphigoid. J Invest Dermatol 85: 72s-78s.
94. Lessey E, Li N, Diaz L, Liu Z, (2008) Complement and cutaneous autoimmune blistering diseases. Immunol Res 41: 223-232.
95. Kawana S, Geoghegan WD, Jordon RE, Nishiyama S, (1989) Deposition of the membrane attack complex of complement in pemphigus vulgaris and pemphigus foliaceus skin. J Invest Dermatol 92: 588-592.
96. Vermeer BJ, Kardaun SH, Koerten HK, Claas FH, Ploem JS, (1985) Model for detection of membrane-associated antigens on epithelial cells (HLA-A,-B,-C alloantigens and pemphigus antigens). Br J Dermatol 113 (Suppl 28): 118-123.
97. Thwaites DT, Anderson CM, (2011) The SLC36 family of proton-coupled amino acid transporters and their potential role in drug transport. British Journal of Pharmacology 164: 1802-1816.
98. Grando SA, (2006) Pemphigus in the XXI Century: New life to an old story. Autoimmunity 39: 521-530.
99. Desai BV, Harmon RM, Green KJ, (2009) Desmosomes at a glance. J Cell Sci 122: 4401-4407.