The polymeric structure of secretory IgM allows efficient antigen binding and complement fixation. The available structural models place the N-glycans bound to asparagines 402 and 563 of Ig-μ chains within a densely packed core of native IgM. These glycans are found in the high mannose state also in secreted IgM, suggesting that polymerization hinders them to Golgi processing enzymes. Their absence alters polymerization. Here we investigate their role following the fate of aggregation-prone mutant μ chains lacking the Cμ1 domain (μΔ). Our data reveal that μΔ lacking 563 glycans (μΔ5) form larger intracellular aggregates than μΔ and are not secreted. Like μΔ, they sequester ERGIC-53, a lectin previously shown to promote polymerization. In contrast, μΔ lacking 402 glycans (μΔ4) remain detergent soluble and accumulate in the ER, as does a double mutant devoid of both (μΔ4-5). These results suggest that the two C-terminal Ig-μ glycans shape the polymerization-dependent aggregation by engaging lectins and acting as spacers in the alignment of individual IgM subunits in native polymers. © The Author(s) 2017.