Abstract
The emergence of the basement membrane (BM), a specialized form of extracellular matrix, was essential in the unicellular transition to multicellularity. However, the mechanism is unknown. Goodpasture antigen-binding protein (GPBP), a BM protein, was uniquely poised to play diverse roles in this transition owing to its multiple isoforms (GPBP-1, -2, and -3) with varied intracellular and extracellular functions (ceramide trafficker and protein kinase). We sought to determine the evolutionary origin of GPBP isoforms. Our findings reveal the presence of GPBP in unicellular protists, with GPBP-2 as the most ancient isoform. In vertebrates, GPBP-1 assumed extracellular function that is further enhanced by membrane-bound GPBP-3 in mammalians, whereas GPBP-2 retained intracellular function. Moreover, GPBP-2 possesses a dual intracellular/extracellular function in cnidarians, an early nonbilaterian group. We conclude that GPBP functioning both inside and outside the cell was of fundamental importance for the evolutionary transition to animal multicellularity and tissue evolution.
Highlights
The emergence of the basement membrane (BM), a specialized form of extracellular matrix, was essential in the unicellular transition to multicellularity
Isoforms lacking an serine repeat motif 2 (SR2) domain were identified across all groups, indicating that Goodpasture antigen– binding protein (GPBP)-2 is conserved across animals, choanoflagellates, and filastereans (Fig. 2B and Fig. S2)
Emerging evidence indicates that BM, an extracellular matrix scaffold composed of numerous proteins, played an essential role in this transition
Summary
The emergence of the basement membrane (BM), a specialized form of extracellular matrix, was essential in the unicellular transition to multicellularity. Recent developmental studies have shifted the view of BM from one of a static support structure to that of a dynamic scaffold that is regularly remodeled to actively shape tissues and direct cell behavior (5, 14 –16). Despite these advances, there is a major gap in knowledge on the composition and function of BM at the transition from unicellular protists to multicellular animals, a pivotal event in metazoan evolution. Recent studies in nonbilaterian animals have shown that collagen IV and laminin [25] are the earliest components of basement membrane, as evidenced in ctenophores and sponges, the two oldest animal lineages, and were likely essential for animal multicellularity [2, 3]
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
