Despite widespread vaccination against Bordetella pertussis (Bp), whooping cough is reemerging. Trafficking receptors (TR) direct cell migration to infection sites, generating protective immunity. To test our hypothesis that pertussis toxin (PTX) modifies dendritic cell (DC) imprinting of TR on T cells, leading to compromised homing to respiratory mucosa, we established a murine model for Bp and B. parapertussis (Bpp)-a strain that lacks PTX and analyzed TR expression by FACS on memory CD4+ CD44+ cells in blood vs lungs during peak infection and recovery (days 5 and 25). While blood memory CD4 cells from Bpp infection revealed 40-100% increased expression of β7, β1, {alpha}4, {alpha}1, {alpha}6, CCR6, CCR5 and CXCR3 at 5 days post infection, while cells from Bp had reduced levels of most TR and expressed {alpha}4 and β1 only later at 25 days post infection. However, expression of β7, {alpha}4, β1 and CCR6 was elevated in lung memory T cells from Bp infected mice at 5 and 25 days post infection, suggesting a local up-regulation of these molecules. In-vitro co-cultures of lung DC from 25 day post infection with Bp but not Bpp resulted in a significant imprinting of {alpha}6, CD103, {alpha}4, β1, CCR6, CD106 and LFA-1. In conclusion, TR imprinting on blood memory T cells is compromised at early Bp infection, however imprinting of TR by DC is efficient at later phase of infection supporting the prolonged manifestation of the natural disease.