Immunological role of keratinocytes in leishmaniasis.


Journal

Parasite immunology
ISSN: 1365-3024
Titre abrégé: Parasite Immunol
Pays: England
ID NLM: 7910948

Informations de publication

Date de publication:
09 2021
Historique:
revised: 13 05 2021
received: 28 11 2020
accepted: 15 05 2021
pubmed: 25 5 2021
medline: 26 11 2021
entrez: 24 5 2021
Statut: ppublish

Résumé

Following inoculation of Leishmania, a protozoan parasite, into the skin of a mammal, the epidermal keratinocytes recognize the parasite and influence the local immune response that can give rise to different outcomes of leishmaniasis. The early keratinocyte-derived cytokines and keratinocytes-T cells interactions shape the anti-leishmanial immune responses that contribute to the resistance or susceptibility to leishmaniasis. The keratinocyte-derived cytokines can directly potentiate the leishmanicidal activity of monocytes and macrophages. As keratinocytes express MHC-II and enhance the expression of costimulatory molecules, these cells act as antigen-presenting cells (APCs) in cutaneous leishmaniasis (CL). Depending on the epidermal microenvironment, the keratinocytes induce various types of effector CD4

Identifiants

pubmed: 34028815
doi: 10.1111/pim.12870
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e12870

Informations de copyright

© 2021 John Wiley & Sons Ltd.

Références

Torres-Guerrero E, Quintanilla-Cedillo MR, Ruiz-Esmenjaud J, Arenas R. Leishmaniasis: a review. F1000Research. 2017;6:750.
Jafarzadeh A, Nemati M, Sharifi I, et al. Leishmania species-dependent functional duality of toll-like receptor 2. IUBMB Life. 2019;71(11):1685-1700.
Jafarzadeh A, Jafarzadeh S, Sharifi I, Aminizadeh N, Nozari P, Nemati M. The importance of T cell-derived cytokines in post-kala-azar dermal leishmaniasis. Cytokine. 2020;155:321.
Jafarzadeh A, Nemati M, Chauhan P, et al. Interleukin-27 functional duality balances leishmania infectivity and pathogenesis. Front Immunol. 2020;11:1573.
Matejuk A. Skin immunity. Arch Immunol Ther Exp. 2018;66(1):45-54.
Salei N, Hellberg L, Kohl J, Laskay T. Enhanced survival of Leishmania major in neutrophil granulocytes in the presence of apoptotic cells. PLoS One. 2017;12(2):e0171850.
Leon B, Lopez-Bravo M, Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity. 2007;26(4):519-531.
Bogdan C. Natural killer cells in experimental and human leishmaniasis. Front Cell Infect Microbiol. 2012;2:69.
Scott P, Novais FO. Cutaneous leishmaniasis: immune responses in protection and pathogenesis. Nat Rev Immunol. 2016;16(9):581-592.
Olekhnovitch R, Ryffel B, Muller AJ, Bousso P. Collective nitric oxide production provides tissue-wide immunity during Leishmania infection. J Clin Investig. 2014;124(4):1711-1722.
Sacks D, Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol. 2002;2(11):845-858.
Cummings HE, Tuladhar R, Satoskar AR. Cytokines and their STATs in cutaneous and visceral leishmaniasis. J Biomed Biotechnol. 2010;2010:294389.
Jafarzadeh A, Larussa T, Nemati M, Jalapour S. T cell subsets play an important role in the determination of the clinical outcome of Helicobacter pylori infection. Microb Pathog. 2018;116:227-236.
Castellano LR, Filho DC, Argiro L, et al. Th1/Th2 immune responses are associated with active cutaneous leishmaniasis and clinical cure is associated with strong interferon-gamma production. Hum Immunol. 2009;70(6):383-390.
Klicznik MM, Szenes-Nagy AB, Campbell DJ, Gratz IK. Taking the lead - how keratinocytes orchestrate skin T cell immunity. Immunol Lett. 2018;200:43-51.
Portou MJ, Baker D, Abraham D, Tsui J. The innate immune system, toll-like receptors and dermal wound healing: A review. Vascul Pharmacol. 2015;71:31-36.
Chauhan P, Shukla D, Chattopadhyay D, Saha B. Redundant and regulatory roles for Toll-like receptors in Leishmania infection. Clin Exp Immunol. 2017;190(2):167-186.
Werfel T. The role of leukocytes, keratinocytes, and allergen-specific IgE in the development of atopic dermatitis. J Invest Dermatol. 2009;129(8):1878-1891.
Shirakata Y. Regulation of epidermal keratinocytes by growth factors. J Dermatol Sci. 2010;59(2):73-80.
Albanesi C, Madonna S, Gisondi P, Girolomoni G. The Interplay Between Keratinocytes and Immune Cells in the Pathogenesis of Psoriasis. Front Immunol. 2018;9:1549.
Asadi A, Tavakoli Kareshk A, Sharifi I, Firouzeh N. Murine cathelicidin: as a host defensive response against Leishmania major infection. J Para Dis. 2020;44(3):633-638.
Fondevila D, Vilafranca M, Ferrer L. Epidermal immunocompetence in canine leishmaniasis. Vet Immunol Immunopathol. 1997;56(3-4):319-327.
Pirmez C, Oliveira-Neto MP, Grimaldi Junior G, Savino W. Immunopathology of American cutaneous leishmaniasis. Modulation of MHC class II gene products by keratinocytes before and after glucantime therapy. Mem Inst Oswaldo Cruz. 1990;85(2):203-209.
de Araújo FF, Costa-Silva MF, Pereira AAS, et al. Chemokines in Leishmaniasis: Map of cell movements highlights the landscape of infection and pathogenesis. Cytokine. 2020;7:155339.
Jafarzadeh A, Nemati M, Jafarzadeh S. The important role played by chemokines influence the clinical outcome of Helicobacter pylori infection. Life Sci. 2019;231:116688.
Quaresma JAS. Organization of the skin immune system and compartmentalized immune responses in infectious diseases. Clin Microbiol Rev. 2019;32(4):e00034-e118.
Kumar A. Pigmentation in Leishmaniasis: Common or Different. Pigm Dis. 2015;2(5):180.
Vasconcellos C, Sotto MN. Experimental cutaneous leishmaniasis: transmission electron microscopy of the inoculation site. Int J Exp Pathol. 1997;78(2):81-89.
Mbow ML, DeKrey GK, Titus RG. Leishmania major induces differential expression of costimulatory molecules on mouse epidermal cells. Eur J Immunol. 2001;31(5):1400-1409.
Scorza BM, Wacker MA, Messingham K, et al. Differential activation of human keratinocytes by leishmania species causing localized or disseminated disease. J Invest Dermatol. 2017;137(10):2149-2156.
Liu D, Uzonna JE. The early interaction of Leishmania with macrophages and dendritic cells and its influence on the host immune response. Front Cell Infect Microbiol. 2012;2:83.
Peters NC, Sacks DL. The impact of vector-mediated neutrophil recruitment on cutaneous leishmaniasis. Cell Microbiol. 2009;11(9):1290-1296.
Olivier M, Gregory DJ, Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev. 2005;18(2):293-305.
Karp CL, Turco SJ, Sacks DL. Lipophosphoglycan masks recognition of the Leishmania donovani promastigote surface by human kala-azar serum. J Immunol. 1991;147(2):680-684.
Pimenta PF, da Silva RP, Sacks DL, da Silva PP. Cell surface nanoanatomy of Leishmania major as revealed by fracture-flip. A surface meshwork of 44 nm fusiform filaments identifies infective developmental stage promastigotes. Eur J Cell Biol. 1989;48(2):180-190.
McCall LI, Zhang WW, Matlashewski G. Determinants for the development of visceral leishmaniasis disease. PLoS Pathog. 2013;9(1):e1003053.
Cumberbatch M, Kimber I. Dermal tumour necrosis factor-alpha induces dendritic cell migration to draining lymph nodes, and possibly provides one stimulus for Langerhans' cell migration. Immunology. 1992;75(2):257-263.
Hurdayal R, Brombacher F. Interleukin-4 receptor alpha: from innate to adaptive immunity in murine models of cutaneous leishmaniasis. Front Immunol. 2017;8:1354.
Teixeira MJ, Teixeira CR, Andrade BB, Barral-Netto M, Barral A. Chemokines in host-parasite interactions in leishmaniasis. Trends Parasitol. 2006;22(1):32-40.
Ribeiro-Gomes FL, Sacks D. The influence of early neutrophil-Leishmania interactions on the host immune response to infection. Front Cell Infect Microbiol. 2012;2:59.
Gasim S, Elhassan AM, Khalil EA, et al. High levels of plasma IL-10 and expression of IL-10 by keratinocytes during visceral leishmaniasis predict subsequent development of post-kala-azar dermal leishmaniasis. Clin Exp Immunol. 1998;111(1):64-69.
Scorza BM, Carvalho EM, Wilson ME. Cutaneous manifestations of human and murine leishmaniasis. Int J Mol Sci. 2017;18(6):1296.
Zijlstra EE, Alves F, Rijal S, Arana B, Alvar J. Post-kala-azar dermal leishmaniasis in the Indian subcontinent: a threat to the South-East Asia Region Kala-azar Elimination Programme. PLoS Negl Trop Dis. 2017;11(11):e0005877.
Nandy A, Addy M, Maji AK, Guha SK, Banerjee D, Chaudhuri D. Recurrence of kala-azar after PKDL: role of co-factors. Trop Med Intern Health. 1998;3(1):76-78.
Kashem SW, Haniffa M, Kaplan DH. Antigen-presenting cells in the skin. Annu Rev Immunol. 2017;35:469-499.
Kaplan G, Nusrat A, Sarno EN, et al. Cellular responses to the intradermal injection of recombinant human gamma-interferon in lepromatous leprosy patients. Am J Pathol. 1987;128(2):345-353.
Pinheiro RO, Schmitz V, Silva BJA, et al. Innate immune responses in leprosy. Front Immunol. 2018;9:518.
Lyrio EC, Campos-Souza IC, Correa LC, et al. Interaction of Mycobacterium leprae with the HaCaT human keratinocyte cell line: new frontiers in the cellular immunology of leprosy. Exp Dermatol. 2015;24(7):536-542.
Ehrchen JM, Roebrock K, Foell D, et al. Keratinocytes determine Th1 immunity during early experimental leishmaniasis. PLoS Pathog. 2010;6(4):e1000871.
McElrath MJ, Kaplan G, Nusrat A, Cohn ZA. Cutaneous leishmaniasis. The defect in T cell influx in BALB/c mice. J Exp Med. 1987;165(2):546-559.
ElHassan AM, Gaafar A, Theander TG. Antigen-presenting cells in human cutaneous leishmaniasis due to Leishmania major. Clin Exp Immunol. 1995;99(3):445-453.
Isaza DM, Restrepo M, Restrepo R, Caceres-Dittmar G, Tapia FJ. Immunocytochemical and histopathologic characterization of lesions from patients with localized cutaneous leishmaniasis caused by Leishmania panamensis. Am J Trop Med Hyg. 1996;55(4):365-369.
Tomiotto-Pellissier F, Bortoleti B, Assolini JP, et al. Macrophage polarization in leishmaniasis: broadening horizons. Front Immunol. 2018;9:2529.
Von Stebut E, Ehrchen JM, Belkaid Y, et al. Interleukin 1alpha promotes Th1 differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. J Exp Med. 2003;198(2):191-199.
von Stebut E. Cutaneous Leishmania infection: progress in pathogenesis research and experimental therapy. Exp Dermatol. 2007;16(4):340-346.
Sunderkotter C, Kunz M, Steinbrink K, et al. Resistance of mice to experimental leishmaniasis is associated with more rapid appearance of mature macrophages in vitro and in vivo. J Immunol. 1993;151(9):4891-4901.
Tacchini-Cottier F, Zweifel C, Belkaid Y, et al. An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J Immunol. 2000;165(5):2628-2636.
Nabors GS, Nolan T, Croop W, Li J, Farrell JP. The influence of the site of parasite inoculation on the development of Th1 and Th2 type immune responses in (BALB/c x C57BL/6) F1 mice infected with Leishmania major. Parasite Immunol. 1995;17(11):569-579.
Constant SL, Brogdon JL, Piggott DA, et al. Resident lung antigen-presenting cells have the capacity to promote Th2 T cell differentiation in situ. J Clin Investig. 2002;110(10):1441-1448.
Roebrock K, Sunderkotter C, Munck NA, et al. Epidermal expression of I-TAC (Cxcl11) instructs adaptive Th2-type immunity. FASEB J. 2014;28(4):1724-1734.
Cui G, Chen J, He J, et al. Osteopontin promotes dendritic cell maturation and function in response to HBV antigens. Drug Des Develop Ther. 2015;9:3003-3016.
Hochrein H, O'Keeffe M, Luft T, et al. Interleukin (IL)-4 is a major regulatory cytokine governing bioactive IL-12 production by mouse and human dendritic cells. J Exp Med. 2000;192(6):823-833.
Biedermann T, Zimmermann S, Himmelrich H, et al. IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nat Immunol. 2001;2(11):1054-1060.
Himmelrich H, Launois P, Maillard I, et al. In BALB/c mice, IL-4 production during the initial phase of infection with Leishmania major is necessary and sufficient to instruct Th2 cell development resulting in progressive disease. Journal of immunology. 2000;164(9):4819-4825.
Kedzierski L, Evans KJ. Immune responses during cutaneous and visceral leishmaniasis. Parasitology. 2014;1-19.
Hurdayal R, Nieuwenhuizen NE, Revaz-Breton M, et al. Deletion of IL-4 receptor alpha on dendritic cells renders BALB/c mice hypersusceptible to Leishmania major infection. PLoS Pathog. 2013;9(10):e1003699.
Descatoire M, Hurrell BP, Govender M, et al. IL-4Ralpha signaling in keratinocytes and early IL-4 production are dispensable for generating a curative T Helper 1 Response in leishmania major-infected C57BL/6 mice. Front Immunol. 2017;8:1265.
Grone A. Keratinocytes and cytokines. Vet Immunol Immunopathol. 2002;88(1-2):1-12.
Junghans V, Jung T, Neumann C. Human keratinocytes constitutively express IL-4 receptor molecules and respond to IL-4 with an increase in B7/BB1 expression. Exp Dermatol. 1996;5(6):316-324.
Lee GR. The balance of Th17 versus treg cells in autoimmunity. Int J Mol Sci. 2018;19(3).
Etesam Z, Nemati M, Ebrahimizadeh MA, et al. Altered expression of specific transcription factors of Th17 (RORgammat, RORalpha) and treg lymphocytes (FOXP3) by peripheral blood mononuclear cells from patients with multiple sclerosis. J Mol Neurosci. 2016;60(1):94-101.
Nylen S, Eidsmo L. Tissue damage and immunity in cutaneous leishmaniasis. Parasite Immunol. 2012;34(12):551-561.
Tasew G, Nylen S, Lieke T, et al. Systemic FasL and TRAIL neutralisation reduce leishmaniasis induced skin ulceration. PLoS Negl Trop Dis. 2010;4(10):e844.
Daehn IS, Varelias A, Rayner TE. T-lymphocyte-induced, Fas-mediated apoptosis is associated with early keratinocyte differentiation. Exp Dermatol. 2010;19(4):372-380.
Eidsmo L, Nylen S, Khamesipour A, Hedblad MA, Chiodi F, Akuffo H. The contribution of the Fas/FasL apoptotic pathway in ulcer formation during Leishmania major-induced cutaneous Leishmaniasis. Am J Pathol. 2005;166(4):1099-1108.
Miramin-Mohammadi A, Javadi A, Eskandari SE, Mortazavi H, Rostami MN, Khamesipour A. Immune response in cutaneous leishmaniasis patients with healing vs. non-healing lesions. Iranian J Microbiol. 2020;12(3):249-255.
Eidsmo L, Fluur C, Rethi B, et al. FasL and TRAIL induce epidermal apoptosis and skin ulceration upon exposure to Leishmania major. Am J Pathol. 2007;170(1):227-239.
Campos TM, Costa R, Passos S, Carvalho LP. Cytotoxic activity in cutaneous leishmaniasis. Mem Inst Oswaldo Cruz. 2017;112(11):733-740.
Abdoli A, Maspi N, Ghaffarifar F. Wound healing in cutaneous leishmaniasis: A double edged sword of IL-10 and TGF-beta. Comp Immunol Microbiol Infect Dis. 2017;51:15-26.
Pastar I, Stojadinovic O, Yin NC, et al. Epithelialization in wound healing: a comprehensive review. Adv Wound Care. 2014;3(7):445-464.
Vargas-Inchaustegui DA, Xin L, Soong L. Leishmania braziliensis infection induces dendritic cell activation, ISG15 transcription, and the generation of protective immune responses. Journal of immunology. 2008;180(11):7537-7545.
Gimblet C, Loesche MA, Carvalho L, et al. IL-22 Protects against tissue damage during cutaneous leishmaniasis. PLoS One. 2015;10(8):e0134698.
Zenewicz LA, Flavell RA. Recent advances in IL-22 biology. Int Immunol. 2011;23(3):159-163.
Boniface K, Bernard FX, Garcia M, Gurney AL, Lecron JC, Morel F. IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J Immunol. 2005;174(6):3695-3702.
Rotty JD, Coulombe PA. A wound-induced keratin inhibits Src activity during keratinocyte migration and tissue repair. J Cell Biol. 2012;197(3):381-389.
Guilloteau K, Paris I, Pedretti N, et al. Skin inflammation induced by the synergistic action of IL-17A, IL-22, oncostatin M, IL-1α, and TNF-α recapitulates some features of psoriasis. J Immunol. 2010;184(9):5263-5270.
Rezvani HR, Ali N, Nissen LJ, et al. HIF-1α in epidermis: oxygen sensing, cutaneous angiogenesis, cancer, and non-cancer disorders. J Invest Dermatol. 2011;131(9):1793-1805.
Charpentier T, Hammami A, Stäger S. Hypoxia inducible factor 1α: A critical factor for the immune response to pathogens and Leishmania. Cell Immunol. 2016;309:42-49.
Schatz V, Strüssmann Y, Mahnke A, et al. Myeloid Cell-Derived HIF-1α promotes control of leishmania major. Journal of immunology. 2016;197(10):4034-4041.
Alonso D, Serrano E, Bermejo FJ, Corral RS. HIF-1α-regulated MIF activation and Nox2-dependent ROS generation promote Leishmania amazonensis killing by macrophages under hypoxia. Cell Immunol. 2019;335:15-21.
Tashiro N, Segawa R, Tobita R, et al. Hypoxia inhibits TNF-α-induced TSLP expression in keratinocytes. PLoS One. 2019;14(11):e0224705.
Covre LP, De Maeyer RPH, Gomes DCO, Akbar AN. The role of senescent T cells in immunopathology. Aging Cell. 2020;19(12):e13272.
Wang Z, Man M-Q, Li T, Elias PM, Mauro TM. Aging-associated alterations in epidermal function and their clinical significance. Aging. 2020;12(6):5551-5565.

Auteurs

Abdollah Jafarzadeh (A)

Department of Immunology, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran.
Molecular Medicine Research Center, Research Institute of Basic Medical Sciences, Rafsanjan University of Medical Sciences, Rafsanjan, Iran.

Arathi Nair (A)

Trident Academy of Creative Technology, Bhubaneswar, India.

Sara Jafarzadeh (S)

Student Research Committee, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran.

Maryam Nemati (M)

Department of Immunology, School of Medicine, Rafsanjan University of Medical Sciences, Rafsanjan, Iran.
Department of Haematology and Laboratory Sciences, School of Para-Medicine, Kerman University of Medical Sciences, Kerman, Iran.

Iraj Sharifi (I)

Leishmaniasis Research Center, Kerman University of Medical Sciences, Kerman, Iran.

Bhaskar Saha (B)

Trident Academy of Creative Technology, Bhubaneswar, India.
National Centre for Cell Science, Pune, India.

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