Evolutionary conservation and association of SPARC with the basal lamina in Drosophila

Abstract

SPARC (secreted protein, acidic, rich in cysteine, also called BM40 and osteonectin) is a multifunctional calcium-binding glycoprotein whose modular organization has been highly conserved between invertebrates and vertebrates, indicating a conservation of function during metazoan evolution. Genome analysis has revealed a single copy of the DrosophilaSPARC ( dSPARC) gene. As a first step towards investigating the function of SPARC in Drosophila, we examined its spatiotemporal distribution during development. During embryogenesis, dSPARC mRNA transcripts are restricted to mesoderm derivatives, hemocytes, and the fat body. Immunostaining with anti- DrosophilaSPARC antibodies indicates that dSPARC secreted by the hemocytes and fat body cells is concentrated in basal laminae surrounding internal organs. During oogenesis, dSPARC transcripts are restricted to the somatic cells of the germarium and follicles. Consistent with embryonic development, the resultant protein is concentrated in basal laminae. Mutations in type IV collagen are associated with a dramatic decrease in dSPARC protein immunostaining in hemocytes. The data suggest that the production and assembly of dSPARC in the basal lamina is dependent on type IV collagen, and raise the possibility that dSPARC and type IV collagen interactions are a prerequisite to the assembly and structural integrity of basal laminae in Drosophila.

Mineralized tissue and vertebrate evolution: The secretory calcium-binding phosphoprotein gene cluster

“…However, this study did not consider the limits of sequence variation in the SP and a subsequent amino acid residue (26). Although SPARCL1 seems to be of recent origin, SPARC is identified in nematode and fruit fly (69). By exon shuffling, SPARC obtained a Follistatin-like domain (70), which is not seen in the other dental (enamel͞ dentine) and bone ECM protein genes in the cluster.…”

SPARC is expressed by macroglia and microglia in the developing and mature nervous system

“…Later, SPARC is ideally positioned to play a role in the formation and maintenance of the basal lamina that is necessary for Schwann cell myelination (Fig. 6) (Court et al, 2006), similar to its role in basement membranes in other tissues and across multiple organisms (Fitzgerald and Schwarzbauer, 1998;Huynh et al, 2000;Bradshaw and Sage, 2001;Martinek et al, 2002). This may also explain why oligodendrocytes, whose myelin does not have a basal lamina, do not express SPARC.…”

“…The SVZ contains specialized structures of extravascular basal lamina, termed fractones, that contain laminin and collagen (Mercier et al, 2002). As a highly conserved base- ment membrane molecule (Fitzgerald and Schwarzbauer, 1998;Bradshaw and Sage, 2001;Martinek et al, 2002), SPARC may be involved in the assembly and maintenance of fractones by regulating the production of ECM molecules such as laminin (Kamihagi et al, 1994;Weaver et al, 2006) and collagen (Francki et al, 1999;Bradshaw et al, 2003b). Ultrastructural examination of SPARC in the SVZ will be necessary to investigate this possibility further.…”

Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae inDrosophilaembryos

“…-binding matricellular glycoprotein whose modular organization is phylogenetically conserved (Martinek et al, 2002). Biochemical studies indicate that SPARC binds to several collagenous and non-collagenous ECM molecules, including a Ca 2+ -dependent interaction with network-forming collagen IV (Maurer et al, 1997;Rosenblatt et al, 1997).…”

“…In addition to serving as adhesive substrata for cell adhesion and migration, basal laminae regulate signal transduction pathways through interactions with cell-surface receptors, such as members of the integrin superfamily (Bokel and Brown, 2002). Whereas the molecular complexity of basal laminae varies among tissues, the most broadly distributed components include laminin, collagen IV, perlecan, nidogen and SPARC (Erickson and Couchman, 2000;Martinek et al, 2002;Quondamatteo, 2002). Mammalian genomes encode six genetically distinct collagen IV α chains (Boutaud et al, 2000).…”