Clathrin Mediated Endocytosis (CME) is the most widespread form of plasma membrane vesicle formation (1), allowing for cargo transport to the cytoplasm, cellular signaling, nutrient uptake, membrane composition regulation, and viral entryway into the cell. It is a core mechanism of cellular biology, and is carried out by a plethora of different yet well known proteins (2). However, a number of CME actors are, to a large degree, intrinsically disordered ; i.e. lacking stable secondary-structure, and comprising fast dynamics, which makes them very challenging to study. We focus on the synaptic intrinsically disordered 91kDa monomeric clathrin assembly protein, AP180. During CME initiation, it has been shown that AP180 interacts with the heterotetrameric CME hub protein complex AP2 (Adaptor Protein 2), as well as with clathrin itself (3), yet, it remains unclear as to how the interaction is accomplished. We characterized the interactions and dynamics at play around AP180 and its partners, using NMR spectroscopy on large intrinsically disordered protein constructs up to its 600 residue-long full length intrinsically disordered region. Titration experiments not only confirmed previously suspected interaction motifs between AP180 and its partners, but also highlighted different functional motifs along the sequence. These new interaction sites were characterized through relaxation and relaxation-dispersion experiments, also involving protein mutants hindering the interaction. This work, through atomic-resolution information on a very dynamic and disordered system, updates existing knowledge regarding the AP180 interactome, and lays the basis for both a better and atomistic understanding of the initial steps of CME, and for the building of more accurate and complete models of synaptic membrane biology.