Human phosphofructokinase-1 (PFK1) forms filaments and organizes into large-scale assemblies that are thought to play a key role in the spatial organization of glycolysis. However, the molecular interactions driving this assembly and the isoform-specific tendencies to form such structures remain poorly understood. In this work, we combine coarse-grained and all-atom molecular dynamics simulations to characterize interactions between PFK1 tetramers. Using the Martini and OPEPv7 coarse-grained force fields, we identify key regions mediating transient PFK1-PFK1 interactions and show that these include experimentally identified filament-forming interfaces. At the same time, we find that current coarse-grained models─optimized for nonspecific, transient contacts─lack the resolution to capture the specific side-chain interactions critical for filament stability, as revealed by previous experiments and our all-atom simulations. To address this, we propose enhancing the coarse-grained representation of filament-forming interfaces by introducing additional hydrogen-bonding terms for key residues. This modification improves filament stability and more accurately reproduces the effects of the filament-disrupting Asn-to-Thr mutation. Overall, our work provides a foundation for molecular-level modeling of glycolytic enzyme assemblies and offers a strategy to improve the accuracy of coarse-grained models in capturing the delicate interplay between specific and transient interactions in dynamic protein complexes.