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A vertebrate ortholog of Shf, the Wnt Inhibitory Factor-1 (WIF-1) has no known role in Hedgehog signaling. Instead, WIF-1 binds and inhibits vertebrate Wnts, and also inhibits Drosophila Wnt member Wingless (Wg), in all circumstances by an unknown mechanism. In contrast, Shf has no known role during Wg signaling. It remains in question whether WIF-1 and Shf have overlapping roles. Therefore we ask whether WIF-1 has a role in Hh signaling, and whether Shf may influence signaling by Wg. We find that HSPGs render WIFI-1 more effective in inhibiting Wnt/Wg in both vertebrates and flies. We also show that the vertebrate Wnt-binding WIF domain helps Hh signaling. Finally, we provide genetic evidence that implicates Shf involvement during Wg signaling. Together these findings reveal unexpected and overlapping roles between WIF-1 and Shf.