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Psoriatic keratinocytes prime neutrophils for an overproduction of superoxide anions

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Abstract

Psoriatic plaques result from an abnormal proliferation of keratinocytes associated with the local presence of T lymphocytes and neutrophils. The exact role of neutrophils in psoriatic lesions remains unclear. The present investigation was aimed at deciphering the capacity of psoriatic keratinocytes to alter in vitro functions of neutrophils. Blood neutrophils from healthy donors were incubated with psoriatic (PK) or healthy keratinocytes (HK) with and without IL-2-activated healthy T lymphocytes. The study was focussed on neutrophil capacity of adherence, viability and superoxide anion production. PK or HK with or without T lymphocytes similarly augmented neutrophil viability after 48 h of co-incubation. PK or HK did not directly activate the superoxide production by neutrophils. However, they both primed neutrophils for an increased fMLF-induced production of superoxide, an effect enhanced by the presence of T lymphocytes. PK were 1.5-fold more efficient than HK to augment this superoxide production. PK cultured with T lymphocytes induced the adhesion of neutrophils 4.7 times more efficiently than HK. The adherence of neutrophils was mediated through ICAM-1, LFA-1 and Mac-1, independently of bioactive lipids. The effects of PK and HK on neutrophil viability and priming were independent of direct cellular contact. In conclusion, keratinocytes can impact neutrophils by increasing their lifespan, and by priming them to overproduce superoxide. PK are more efficient than HK in priming neutrophils, an effect enhanced by T lymphocytes. These results indicate that neutrophils could contribute to psoriasis pathogenesis partly through their pathological interactions with PK.

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Abbreviations

cPLA2 :

Cytosolic phospholipase A2

GM-CSF:

Granulocyte-macrophage-colony-stimulating factor

HK:

Healthy keratinocytes

ICAM-1:

Intercellular adhesion molecule-1

LFA-1:

Lymphocyte function-associated antigen 1

LTB4 :

Leukotriene B4

O2 − :

Superoxide anion

PAF:

Platelet-activating factor

PI:

Propidium iodide

PK:

Psoriatic keratinocytes

ROS:

Reactive oxygen species

TNF-α:

Tumor necrosis factor-α

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Acknowledgments

We thank Dr. Jacques Soucy (Département de Dermatologie, Hôpital de l’Enfant-Jésus, Québec) for his help in providing us with biopsies of chronic plaque from patients affected by psoriasis vulgaris. This study was supported by a grant from the Canadian Institutes of Health Research (CIHR) to Drs R. Pouliot and P.E. Poubelle. Dr R Pouliot was recipient of a research fellowship from the “Fonds de la Recherche en Santé du Québec”. S Guérard received a graduate scholarship from the “Fonds de Recherche en Santé du Québec” and from the “Fonds d’enseignement et de recherche” of the Faculté de Pharmacie of Université Laval.

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SG, IA, GM, RP and PEP declare no conflict of interest.

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Authors and Affiliations

  1. Laboratoire d’Organogénèse Expérimentale (LOEX), Centre de Recherche FRSQ du CHU de Québec, Québec, Canada

    Simon Guérard, Guillaume Martin & Roxane Pouliot

  2. Centre de Recherche en Rhumatologie et Immunologie, CRCHUL, Centre de Recherche du CHU de Québec, 2705 Blvd Laurier, T1-49, Québec, QC, G1V 4G2, Canada

    Simon Guérard, Isabelle Allaeys, Guillaume Martin & Patrice E. Poubelle

  3. Faculté de Pharmacie, Université Laval, Québec, Canada

    Simon Guérard & Roxane Pouliot

  4. Département de Médecine, Faculté de Médecine, Université Laval, Québec, Canada

    Isabelle Allaeys & Patrice E. Poubelle

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  1. Simon Guérard
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Correspondence to Patrice E. Poubelle.

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Guérard, S., Allaeys, I., Martin, G. et al. Psoriatic keratinocytes prime neutrophils for an overproduction of superoxide anions. Arch Dermatol Res 305, 879–889 (2013). https://doi.org/10.1007/s00403-013-1404-z

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