Lipids participate in cellular homeostasis through selective interactions with proteins, by functioning as second messengers in signaling processes and through the generation of cellular compartments to transfer cargo between organelles. The focus of this thesis is on the peripheral protein cytosolic phospholipase A2 α (cPLA2α) that participates in all three of these functions of lipids.  cPLA2α generates the lipid metabolite arachidonic acid (AA) by hydrolyzing phosphatidylcholine at the sn-2 position. AA is then further metabolized by cyclooxygenase (COX) 1 and COX 2 to generate prostaglandins (PGs) and by lipoxygenases to generate leukotrienes (LTs), which play both homeostatic and pathological roles. This cPLA2α signaling has been implicated in cancer, allergy, asthma, arthritis and heart disease, causing cPLA2α to become a high profile therapeutic target in the literature. The enzyme is composed of two domains: A C-terminal catalytic domain and an N-terminal lipid binding conserved 2 (C2) domain. Our initial aim was focused on developing a better understanding of the ceramide-1-phosphate (C1P) recognition within the cPLA2α C2 domain, as it has been implicated in the regulation of the enzyme's activity. In this study, we identified the molecular basis of the first C1P binding site primarily through the basic residues Arg59, Arg 61 and His62. In addition, we have helped collaborators to identify and characterize other selective C1P binding proteins. During the course of these studies, we found that cPLA2α is also capable of generating cellular vesicles proposed to be involved in trafficking cargo from the Golgi apparatus to the plasma membrane, which is supported by several other reports in the literature. Seeing that the C2 domain of cPLA2α was only one of three C2 domains shown to bend membranes, we began a mechanistic study to better understand C2 domain-dependent membrane bending. We found that cPLA2α C2 domain penetration into the membrane is a critical component of the protein's ability to bend membranes in vitro. Our recent work delivered evidence supporting the formation of large protein oligomers through the C2 domain that are capable of sensing and inducing membrane bending through a novel mechanism for C2 lipid binding domains. These experimental findings have already been utilized to better understand C1P binding and have improved our understanding of this tightly regulated protein and its function in vivo.  This work has provided the groundwork necessary to develop a selective cPLA2α inhibitor that is capable of recognizing cPLA2α over other phospholipases by targeting the C1P binding site. Through further analysis of the particular residues responsible for oligomerization, cPLA2α could maintain its homeostatic function in vesicular trafficking after treatment with the therapeutic. This knowledge of the enzyme's structure and function provide insight to develop an optimal therapeutic inhibitor. This model therapeutic would retain membrane-bending capabilities while decreasing catalytic activity of the enzyme, which has been linked to pathological roles in cancer, asthma, arthritis and heart disease.