Plasmacytoid dendritic cells in dermatology<sup>,</sup>

Dias de Oliveira, Natasha Favoretto; Santi, Claudia Giuli; Maruta, Celina Wakisaka; Aoki, Valeria

doi:10.1016/j.abd.2020.08.006

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Review • An. Bras. Dermatol. 96 (1) • Jan-Feb 2021 • https://doi.org/10.1016/j.abd.2020.08.006 copy

Plasmacytoid dendritic cells in dermatology^☆ ☆ How to cite this article: Dias de Oliveira NF, Santi CG, Maruta CW, Aoki V. Plasmacytoid dendritic cells in dermatology. An Bras Dermatol. 2021;96:76-81. ^,^☆☆ ☆☆ Study conducted at the Department of Dermatology, Faculty of Medicine, Universidade de São Paulo, São Paulo, SP, Brasil.

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Plasmacytoid dendritic cells are part of the dendritic cells family and are a relevant link between innate and adaptive immunity. They are the most potent producers of type 1 interferon, generating antiviral response, stimulating macrophages and dendritic cells and inducing activation and migration of natural killer cells. Plasmacytoid dendritic cells also exert a role as antigen-presenting cells, promote T-lymphocyte responses, immunoregulation, plasma cells differentiation and antibody secretion. Even though plasmacytoid dendritic cells are not usually present in normal skin, their presence is detected in healing processes, viral infections, and inflammatory, autoimmune, and neoplastic diseases. In recent years, the presence of plasmacytoid dendritic cells in several dermatological diseases has been described, enhancing their potential role in the pathogenesis of such conditions. Future studies on the role of plasmacytoid dendritic cells in dermatology may lead to new therapeutic targets.

KEYWORDS
Adaptive immunity; Dendritic cells; Dermatological diseases; Dermatology; Innate immunity

Dermatological diseases	pDCs
Lupus erythematosus	SLE: reduced circulating pDCs³3 Tomasini D, Mentzel T, Hantschke M, Cerri A, Paredes B, Rütten A, et al. Plasmacytoid dendritic cells: an overview of their presence and distribution in different inflammatory skin diseases, with special emphasis on Jessner’s lymphocytic infiltrate of the skin and cutaneous lupus erythematosus. J Cutan Pathol. 2010;37:1132-9.^,¹¹11 McNiff JM, Kaplan DH. Plasmacytoid dendritic cells are present in cutaneous dermatomyositis lesions in a pattern distinct from lupus erythematosus. J Cutan Pathol. 2008;35:452-6. 12 Rowland SL, Riggs JM, Gilfillan S, Bugatti M, Vermi W, Kolbeck R, et al. Early, transient depletion of plasmacytoid dendritic cells ameliorates autoimmunity in a lupus model. J Exp Med. 2014;211:1977-91.^-¹³13 Walsh NM, Lai J, Hanly JG, Green PJ, Bosisio F, Garcias-Ladaria J, et al. Plasmacytoid dendritic cells in hypertrophic discoid lupus erythematosus: an objective evaluation of their diagnostic value. J Cutan Pathol. 2015;42:32-8.
	DL: large amounts of IFN-α producing pDCs³3 Tomasini D, Mentzel T, Hantschke M, Cerri A, Paredes B, Rütten A, et al. Plasmacytoid dendritic cells: an overview of their presence and distribution in different inflammatory skin diseases, with special emphasis on Jessner’s lymphocytic infiltrate of the skin and cutaneous lupus erythematosus. J Cutan Pathol. 2010;37:1132-9.^,¹¹11 McNiff JM, Kaplan DH. Plasmacytoid dendritic cells are present in cutaneous dermatomyositis lesions in a pattern distinct from lupus erythematosus. J Cutan Pathol. 2008;35:452-6. 12 Rowland SL, Riggs JM, Gilfillan S, Bugatti M, Vermi W, Kolbeck R, et al. Early, transient depletion of plasmacytoid dendritic cells ameliorates autoimmunity in a lupus model. J Exp Med. 2014;211:1977-91.^-¹³13 Walsh NM, Lai J, Hanly JG, Green PJ, Bosisio F, Garcias-Ladaria J, et al. Plasmacytoid dendritic cells in hypertrophic discoid lupus erythematosus: an objective evaluation of their diagnostic value. J Cutan Pathol. 2015;42:32-8.
	SAL, DL: superficial distribution³3 Tomasini D, Mentzel T, Hantschke M, Cerri A, Paredes B, Rütten A, et al. Plasmacytoid dendritic cells: an overview of their presence and distribution in different inflammatory skin diseases, with special emphasis on Jessner’s lymphocytic infiltrate of the skin and cutaneous lupus erythematosus. J Cutan Pathol. 2010;37:1132-9.
	TL, MHR: distribution around deep vessels³3 Tomasini D, Mentzel T, Hantschke M, Cerri A, Paredes B, Rütten A, et al. Plasmacytoid dendritic cells: an overview of their presence and distribution in different inflammatory skin diseases, with special emphasis on Jessner’s lymphocytic infiltrate of the skin and cutaneous lupus erythematosus. J Cutan Pathol. 2010;37:1132-9.
	pDCs localized preferably in the epidermis in patients with DM and in the dermis in cases of lupus¹¹11 McNiff JM, Kaplan DH. Plasmacytoid dendritic cells are present in cutaneous dermatomyositis lesions in a pattern distinct from lupus erythematosus. J Cutan Pathol. 2008;35:452-6.
Lichen planus	pDCs arranged similarly to the band-like lymphocytic infiltrate at the dermo-epidermal junction¹⁶16 de Vries HJ, van Marle J, Teunissen MB, Picavet D, Zorgdrager F, Bos JD, et al. Lichen planus is associated with human herpesvirus type 7 replication and infiltration of plasmacytoid dendritic cells. Br J Dermatol. 2006;154:361-4.^,¹⁷17 de Vries HJ, Teunissen MB, Zorgdrager F, Picavet D, Cornelissen M. Lichen planus remission is associated with a decrease of human herpes virus type 7 protein expression in plasmacytoid dendritic cells. Arch Dermatol Res. 2007;299:213-9.
	pDCs increased in oral lichen planus¹⁸18 Wang Y, Shang S, Sun Q, Chen J, Du G, Nie H, et al. Increased infiltration of CD11 c+/CD123+ dendritic cell subsets and upregulation of TLR/IFN-α signaling participate in pathogenesis of oral lichen planus. Oral Surg Oral Med Oral Pathol Oral Radiol. 2018;125:459-67.
Lichen striatus	pDCs present in the inflammatoryinfiltrate
	Perieccrine distribution of pDCs¹⁹19 Badr D, Abadi R, Kurban M, Abbas O. Plasmacytoid Dendritic Cells and Type I Interferon Signature in Lichen Striatus. Pediatr Dermatol. 2016;33:301-6.
Atopic dermatitis	Increased circulating pDCs compared to controls
	Lower recruitment of pDCs in AD lesions compared to other dermatoses, such as lupus erythematosus and psoriasis²⁰20 Novak N, Bieber T. The role of dendritic cell subtypes in the pathophysiology of atopic dermatitis. J Am Acad Dermatol. 2005;53(2 Suppl 2):S171-6.^,²¹21 Wollenberg A, Wagner M, Günther S, Towarowski A, Tuma E, Moderer M, et al. Plasmacytoid dendritic cells: a new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J Invest Dermatol. 2002;119:1096-102.
Polymorphic light eruption	Wackernagel et al.:²²22 Wackernagel A, Massone C, Hoefler G, Steinbauer E, Kerl H, Wolf P. Plasmacytoid dendritic cells are absent in skin lesions of polymorphic light eruption. Photodermatol Photoimmunol Photomed. 2007;23:24-8. absent pDCs
	Rossi et al.:²³23 Rossi MT, Arisi M, Lonardi S, Lorenzi L, Ungari M, Serana F, et al. Cutaneous infiltration of plasmacytoid dendritic cells and T regulatory cells in skin lesions of polymorphic light eruption. J Eur Acad Dermatol Venereol. 2018;32:985-91. increased pDCs in PLE lesions, mainly dermal. The authors attribute the difference to the methodology witch included of a photoprovocation testing.
Psoriasis	pDCs present in the T lymphocyte infiltrate in the dermis of psoriatic plaques and in the perilesional skin²⁴24 Nestle FO, Conrad C, Tun-Kyi A, Homey B, Gombert M, Boyman O, et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med. 2005;202:135-43.
	Reduction of pDCs in the peripheral blood of patients with psoriasis²⁴24 Nestle FO, Conrad C, Tun-Kyi A, Homey B, Gombert M, Boyman O, et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med. 2005;202:135-43.
	Heliotherapy: reduction of pDCs amount and MxA expression²⁵25 Heier I, Søyland E, Krogstad AL, Rodríguez-Gallego C, Nenseter MS, Jahnsen FL. Sun exposure rapidly reduces plasmacytoid dendritic cells and inflammatory dermal dendritic cells in psoriatic skin. Br J Dermatol. 2011;165:792-801.
	Strong chemerin expression and presence of pDCs in the perilesional skin dermis²⁶26 Albanesi C, Scarponi C, Pallotta S, Daniele R, Bosisio D, Madonna S, et al. Chemerin expression marks early psoriatic skin lesions and correlates with plasmacytoid dendritic cell recruitment. J Exp Med. 2009;206:249-58.
Pityriasis lichenoides	Strong MxA expression in PL lesions (local production of type 1 IFN)²⁷27 Wenzel J, Gütgemann I, Distelmaier M, Uerlich M, Mikus S, Bieber T, et al. The role of cytotoxic skin-homing CD8+ lymphocytes in cutaneous cytotoxic T-cell lymphoma and pityriasis lichenoides. J Am Acad Dermatol. 2005;53:422-7.^,²⁸28 Haller O, Kochs G. Human MxA protein: an interferon- induced dynamin-like GTPase with broad antiviral activity. J Interferon Cytokine Res. 2011;31:79-87.
	Presence of pDCs on the skin in all cases (PLEVA and PLC)²⁹29 Karouni M, Rahal JA, Kurban M, Kibbi AG, Abbas O. Possible role of plasmacytoid dendritic cells in pityriasis lichenoides. Clin Exp Dermatol. 2018;43:404-9.
Graft vs. host disease	Presence of pDCs in skin fragments of patients with acute GVHD, strong expression of MxA, signaling local production of type 1 IFN³⁰30 Malard F, Bossard C, Brissot E, Chevallier P, Guillaume T, Delaunay J, et al. Increased plasmacytoid dendritic cells and RORγt-expressing immune effectors in cutaneous acute graft-versus-host disease. J Leukoc Biol. 2013;94:1337-43.
	Reduction of serum pDCs in patients with acute GVHD³¹31 Mohty M, Blaise D, Faucher C, Bardou VJ, Gastaut JA, Viens P, et al. Impact of plasmacytoid dendritic cells on outcome after reduced-intensity conditioning allogeneic stem cell transplantation. Leukemia. 2005;19:1-6.
	Presence of CD123+ cells in the oral mucosa of patients with chronic GVHD was not superior³²32 Botari CM, Nunes AJ, Souza MP, Orti-Raduan ES, Salvio AG. Oral chronic graft-versus-host disease: analysis of dendritic cells subpopulations. An Bras Dermatol. 2014;89:632-7.
Warts	Saadeh et al.:³³33 Saadeh D, Kurban M, Abbas O. Plasmacytoid dendritic cells and type I interferon in the immunological response against warts. Clin Exp Dermatol. 2017;42:857-62. activated pDCs in inflamed viral warts, contrary to what was found by Tomasini et al.³3 Tomasini D, Mentzel T, Hantschke M, Cerri A, Paredes B, Rütten A, et al. Plasmacytoid dendritic cells: an overview of their presence and distribution in different inflammatory skin diseases, with special emphasis on Jessner’s lymphocytic infiltrate of the skin and cutaneous lupus erythematosus. J Cutan Pathol. 2010;37:1132-9. (possible differences in histologic criteria for inflamed warts).
	Reduction in pDCs in peripheral blood and in skin lesions, absence of type 1 IFN production (MxA without expression) in patients with WHIM syndrome³⁴34 Tassone L, Moratto D, Vermi W, De Francesco M, Notarangelo LD, Porta F, et al. Defect of plasmacytoid dendritic cells in warts, hypogammaglobulinemia, infections, myelokathexis (WHIM) syndrome patients. Blood. 2010;116:4870-3.
Fungal diseases	pDCs found in 37% of the skin fragments of patients with CBM and in 50% of the specimens from patients with PCM, but absent in cases of lobomycosis³⁵35 Pagliari C, Kanashiro-Galo L, Silva AA, Barboza TC, Criado PR, Duarte MI, et al. Plasmacytoid dendritic cells in cutaneous lesions of patients with chromoblastomycosis, lacaziosis, and paracoccidioidomycosis: a comparative analysis. Med Mycol. 2014;52:397-402.
Leprosy	Massone et al.:³⁶36 Massone C, Nunzi E, Ribeiro-Rodrigues R, Talhari C, Talhari S, Schettini AP, et al. T regulatory cells and plasmocytoid dendritic cells in Hansen disease: a new insight into pathogenesis?. Am J Dermatopathol. 2010;32:251-6. absence of CD123 expression, except for focal expression in two cases of erythema nodosum leprosum
	Hirai et al.:³⁷37 Hirai KE, Aarão TL, Silva LM, de Sousa JR, de Souza J, Dias LB, et al. Langerhans cells (CD1a and CD207), dermal dendrocytes (FXIIIa) and plasmacytoid dendritic cells (CD123) in skin lesions of leprosy patients. Microb Pathog. 2016;91:18-25. pDCs in the inflammatory infiltrate and around the vessels. Higher number of pDCs in tuberculoid cases compared to virchowian cases.
Skin tumors	Keratoacanthoma: presence of pDCs in 100% of cases³⁸38 Abbas O, Hussein L, Kurban M, Kibbi AG. Plasmacytoid dendritic cell involvement in the host response against keratoacanthoma. J Am Acad Dermatol. 2014;70:1142-5.
	SCC: presence of pDCs in 90% of cases³⁸38 Abbas O, Hussein L, Kurban M, Kibbi AG. Plasmacytoid dendritic cell involvement in the host response against keratoacanthoma. J Am Acad Dermatol. 2014;70:1142-5.
	AK: correlation between the amount of pDCs recruited in the lesions during treatment with imiquimod and the therapeutic effect of the drug⁴⁰40 Ogawa Y, Kawamura T, Matsuzawa T, Aoki R, Shimada S. Recruitment of plasmacytoid dendritic cells to skin regulates treatment responsiveness of actinic keratosis to imiquimod. J Dermatol Sci. 2014;76:67-9.
	BCC: presence of activated pDCs producing IFN-α in the peritumoral infiltrate during treatment with imiquimod⁴¹41 Stary G, Bangert C, Tauber M, Strohal R, Kopp T, Stingl G. Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J Exp Med. 2007;204:1441-51.
	Melanoma: pDCs arranged around the vessels and close to the tumor cells, but not activated. Presence associated with tumor growth. pDCs activated in cases of regressive melanoma⁴²42 Di Domizio J, Demaria O, Gilliet M. Plasmacytoid dendritic cells in melanoma: can we revert bad into good?. J Invest Dermatol. 2014;134:1797-800.
	KS: pDCs present in 90% of cases, but reduced expression of MxA (possible suppression of pDCs by KSHV)⁴³43 Karouni M, Kurban M, Abbas O. Plasmacytoid dendritic cells in skin lesions of classic Kaposi’s sarcoma. Arch Dermatol Res. 2016;308:487-92.

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[1] * Corresponding author. E-mail: natasha.favoretto@gmail.com (N.F. Dias de Oliveira).