Epidermal keratinocytes initiate wound healing and pro-inflammatory immune responses following percutaneous schistosome infection

Angeli, 2001, Role of the parasite-derived prostaglandin D-2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection, J. Exp. Med., 193, 1135, 10.1084/jem.193.10.1135 Arlian, 1996, Production of IL-1 alpha and IL-1 beta by human skin equivalents parasitized by Sarcoptes scabiei, J. Parasitol., 82, 719, 10.2307/3283881 Baker, 2003, Normal keratinocytes express Toll-like receptors (TLRs) 1, 2 and 5: modulation of TLR expression in chronic plaque psoriasis, Br. J. Dermatol., 148, 670, 10.1046/j.1365-2133.2003.05287.x Barker, 2004, Chapter 19: epidermis as a proinflammatory organ, 439 Blanpain, 2009, Epidermal homeostasis: a balancing act of stem cells in the skin, Nat. Rev. Mol. Cell Biol., 10, 207, 10.1038/nrm2636 Caldelari, 2000, Long-term culture of murine epidermal keratinocytes, J. Invest. Dermatol., 114, 1064, 10.1046/j.1523-1747.2000.00960-4.x Canady, 2013, Increased KGF expression promotes fibroblast activation in a double paracrine manner resulting in cutaneous fibrosis, J. Invest. Dermatol., 133, 647, 10.1038/jid.2012.389 Cook, 2011, Multiple helminth infection of the skin causes lymphocyte hypo-responsiveness mediated by Th2 conditioning of dermal myeloid cells, PLoS Pathog., 7, e1001323, 10.1371/journal.ppat.1001323 Curwen, 2006, Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry, Mol. Cell. Proteomics, 5, 835, 10.1074/mcp.M500313-MCP200 Freedberg, 2001, Keratins and the keratinocyte activation cycle, J. Invest. Dermatol., 116, 633, 10.1046/j.1523-1747.2001.01327.x Gause, 2013, Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths, Nat. Rev. Immunol., 13, 607, 10.1038/nri3476 Haas, 2009, Penetration of cercariae into the living human skin: Schistosoma mansoni vs. Trichobilharzia szidati, Parasitol. Res., 105, 1061, 10.1007/s00436-009-1516-8 Harn, 2009, Modulation of host immune responses by helminth glycans, Immunol. Rev., 230, 247, 10.1111/j.1600-065X.2009.00799.x Harper, 2009, Th17 cytokines stimulate CCL20 expression in keratinocytes in vitro and in vivo: implications for psoriasis pathogenesis, J. Invest. Dermatol., 129, 2175, 10.1038/jid.2009.65 Hogg, 2003, Interleukin-12 p40 secretion by cutaneous CD11c+ and F4/80+ cells is a major feature of the innate immune response in mice that develop Th1-mediated protective immunity to Schistosoma mansoni, Infect. Immun., 71, 3563, 10.1128/IAI.71.6.3563-3571.2003 Hogg, 2003, IL-10 regulates early IL-12-mediated immune responses induced by the radiation-attenuated schistosome vaccine, Int. Immunol., 15, 1451, 10.1093/intimm/dxg142 Hong, 2001, Proinflammatory chemokine induction in keratocytes and inflammatory cell infiltration into the cornea, Invest. Ophtholmol. Vis. Sci., 42, 2795 Hsu, 2011, Dynamics between stem cells, niche, and progeny in the hair follicle, Cell, 144, 92, 10.1016/j.cell.2010.11.049 Hsu, 2012, A family business: stem cell progeny join the niche to regulate homeostasis, Nat. Rev. Mol. Cell Biol., 13, 103, 10.1038/nrm3272 Ingram, 2011, Proteomic analysis of human skin treated with larval schistosome peptidases reveals distinct invasion strategies among species of blood flukes, PLoS Negl. Trop. Dis., 5, e1337, 10.1371/journal.pntd.0001337 Jenkins, 2005, Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways, Int. Immunol., 17, 1409, 10.1093/intimm/dxh319 Jenkins, 2005, Modulation of the host’s immune response by schistosome larvae, Parasite Immunol., 27, 385, 10.1111/j.1365-3024.2005.00789.x Jenkins, 2005, Dendritic cells activated with products released by schistosome larvae drive Th2-type immune responses, which can be inhibited by manipulation of CD40 costimulation, Infect. Immun., 73, 395, 10.1128/IAI.73.1.395-402.2005 Jensen, 2008, A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus, J. Cell Sci., 121, 609, 10.1242/jcs.025502 Kaur, 2000, Adhesive properties of human basal epidermal cells: An analysis of keratinocyte stem cells, transit amplifying cells, and postmitotic differentiating cells, J. Invest. Dermatol., 114, 413, 10.1046/j.1523-1747.2000.00884.x King, 2008, The unacknowledged impact of chronic schistosomiasis, Chronic Illn., 4, 65, 10.1177/1742395307084407 King, 2005, Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis, Lancet, 365, 1561, 10.1016/S0140-6736(05)66457-4 Knudsen, 2005, Proteomic analysis of Schistosoma mansoni cercarial secretions, Mol. Cell. Proteomics, 4, 1862, 10.1074/mcp.M500097-MCP200 Kourilova, 2004, The severity of mouse pathologies caused by the bird schistosome Trichobilharzia regenti in relation to host immune status, Parasitol. Res., 93, 8, 10.1007/s00436-004-1079-7 Kumkate, 2007, CD207+ Langerhans cells constitute a minor population of skin-derived antigen-presenting cells in the draining lymph node following exposure to Schistosoma mansoni, Int. J. Parasitol., 37, 209, 10.1016/j.ijpara.2006.10.007 Lamb, 2013, Keratinocytes propagated in serum-free, feeder-free culture conditions fail to form stratified epidermis in a reconstituted skin model, PLoS One, 8, e52494, 10.1371/journal.pone.0052494 Lichti, 2008, Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice, Nat. Protoc., 3, 799, 10.1038/nprot.2008.50 Maas-Szabowski, 2000, Keratinocyte growth regulation in defined organotypic cultures through IL-1-induced keratinocyte growth factor expression in resting fibroblasts, J. Invest. Dermatol., 114, 1075, 10.1046/j.1523-1747.2000.00987.x Madison, 2003, Barrier function of the skin: “La raison d’etre” of the epidermis, J. Invest. Dermatol., 121, 231, 10.1046/j.1523-1747.2003.12359.x Martin, 1997, Wound healing – aiming for perfect skin regeneration, Science, 276, 75, 10.1126/science.276.5309.75 McKerrow, 1985, Proteinases from invasive larvae of the trematode parasite Schistosoma mansoni degrade connective-tissue and basement-membrane macromolecules, Biochem. J., 231, 47, 10.1042/bj2310047 Mountford, 2004, Schistosomes in the skin: a balance between immune priming and regulation, Trends Parasitol., 20, 221, 10.1016/j.pt.2004.03.003 Muller, 2008, Outside-in signaling through integrins and cadherins: a central mechanism to control epidermal growth and differentiation?, J. Invest. Dermatol., 128, 501, 10.1038/sj.jid.5701248 Mullins, 2009, Extracts of Sarcoptes scabiei De Geer downmodulate secretion of IL-8 by skin keratinocytes and fibroblasts and of GM-CSF by fibroblasts in the presence of proinflammatory cytokines, J. Med. Entomol., 46, 845, 10.1603/033.046.0415 Nagao, 2012, Stress-induced chemokine production by hair follicles recruit Langerhans cell precursors to skin, J. Invest. Dermatol., 132 Paveley, 2009, Fluorescent imaging of antigen released by a skin-invading helminth reveals differential uptake and activation profiles by antigen presenting cells, PLoS NTDs, 3, e528 Paveley, 2011, The Mannose Receptor (CD206) is an important pattern recognition receptor (PRR) in the detection of the infective stage of the helminth Schistosoma mansoni and modulates IFNγ production, Int. J. Parasitol., 41, 1335, 10.1016/j.ijpara.2011.08.005 Pivarcsi, 2003, Expression and function of Toll-like receptors 2 and 4 in human keratinocytes, Int. Immunol., 15, 721, 10.1093/intimm/dxg068 Plikus, 2012, Epithelial stem cells and implications for wound repair, Semin. Cell Dev. Biol., 23, 946, 10.1016/j.semcdb.2012.10.001 Ramalingam, 2009, Regulation of helminth-induced Th2 responses by thymic stromal lymphopoietin, J. Immunol., 182, 6452, 10.4049/jimmunol.0900181 Ramaswamy, 1995, Modulation of IL-1a, IL-1B and IL-1RA production in human keratinocytes by schistosomula of Schistosoma mansoni, Immun. Infect. Dis., 5, 100 Ramaswamy, 1995, Secretion of an anti-inflammatory, immunomodulatory factor by schistosomula of Schistosoma mansoni, J. Inflamm., 46, 13 Smithgall, 2008, IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells, Int. Immunol., 20, 1019, 10.1093/intimm/dxn060 Standen, 1953, The penetration of the cercariae of Schistosoma mansoni into the skin and lymphatics of the mouse, Trans. R. Soc. Trop. Med. Hyg., 47, 292, 10.1016/0035-9203(53)90051-0 Trempus, 2003, Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34, J. Invest. Dermatol., 120, 501, 10.1046/j.1523-1747.2003.12088.x Vollmers, 2012, Two- and three-dimensional culture of keratinocyte stem and precursor cells derived from primary murine epidermal cultures, Stem Cell Rev. Rep., 8, 402, 10.1007/s12015-011-9314-y Wheater, 1979, Schistosoma mansoni: a histological study of migration in the laboratory mouse, Parasitology, 79, 49, 10.1017/S0031182000051970 Wollina, 2004, Candida albicans – induced inflammatory response in human keratinocytes, Mycoses, 47, 193, 10.1111/j.1439-0507.2004.00976.x Wood, 1992, Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice, J. Clin. Invest., 90, 482, 10.1172/JCI115884