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Human Milk-Derived B Cells: A Highly Activated Switched Memory Cell Population Primed to Secrete Antibodies¹

Edouard Tuaillon^2,*, Diane Valea^2,*,, Pierre Becquart^3,*, Yassine Al Tabaa^*, Nicolas Meda, Karine Bollore^*, Philippe Van de Perre^4,* and Jean-Pierre Vendrell^4,*,

^* Unité de Recherche EA 4205, "Transmission, Pathogenèse et Prévention de l’Infection par le VIH", Université Montpellier 1, and Laboratoire de Virologie, Centre Hospitalier Universitaire de Montpellier, Montpellier, France; Centre Muraz, Bobo-Dioulasso, Burkina-Faso; and Institut National de la Santé et de la Recherche Médicale Unité 847, Montpellier, France

While secretory Abs have been extensively explored in human breast milk, the existence, features, and functions of B lymphocytes remain largely unexplored in this compartment. We analyzed breast milk and blood lymphocytes from 21 lactating women, including 12 HIV-1-infected mothers. Breast milk B cells displayed a phenotype of class-switched memory B cells, with few IgD⁺ memory and naive B cells. We observed that breast milk B lymphocytes bore a unique profile of adhesion molecules (CD44⁺, CD62L^–, ₄β₇^+/–, ₄β₁⁺). Higher percentages of activated B cells (CD38⁺), large-sized B cells, plasmablasts, and plasma cells (CD19⁺, CD20^low/–, CD27^high, CD138⁺) were found as compared with blood. This indicates that a significant proportion of breast milk B cells underwent terminal plasma cell differentiation. We also observed a higher frequency of cells secreting Ig spontaneously in breast milk. Among these cells, IgG-secreting cells predominated over IgA-secreting cells as measured by Ig ELISPOT assays. Specific Ab-secreting cells were investigated following polyclonal activation using the CD40L ligation. Finally, the detection of anti-HIV-1-secreting cells demonstrates the existence of B cells specific to HIV-1 Ag in breast milk from HIV-1-infected women. Breast milk B cells display a phenotype strikingly different from blood, are primed to secrete Abs, and have a mucosal homing profile similar to B cells located in gut-associated lymphoid tissue.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This work was supported by the Agence Nationale de Recherches sur le SIDA et les Hépatites Virales (ANRS 1271). The French ministry of foreign affairs supported the Ph.D. grant of Diane Valea, and Beckman Coulter France provided laboratory reagents.

² E.T. and D.V. contributed equally to this work.

³ Current address: Institut de Recherche pour le Développement, Unité Mixte de Recherche 190, Centre International de Recherches Médicales de Franceville, Franceville, Gabon.

⁴ Address correspondence and reprint requests to Dr. Philippe Van de Perre and Dr. Jean-Pierre Vendrell, Laboratoire de Bactériologie-Virologie, Centre Hospitalier Universitaire de Montpellier, 371 avenue du Doyen Gaston Giraud, 34295-Montpellier Cedex 5, France. E-mail addresses: p-van_de_perre{at}chu-montpellier.fr and jp-vendrell{at}chu-montpellier.fr

⁵ Abbreviations used in this paper: IgSC, Ig-secreting cell; ASC, Ab-secreting cell; BMC, breast milk cell; ECD, energy-coupled dye; IQR, interquartile range; MAdCAM-1, mucosal addressin cell adhesion molecule-1; PC5, PE-cyanine 5; PC7, PE-cyanine 7.

⁶ The online version of this article contains supplemental material.