Bone is a dynamic mineralized tissue that undergoes continuous remodeling throughout life. While the general mechanism of bone mineral metabolism is documented, the role of collagen structures in regulating osteoblastic mineral deposition and osteoclastic mineral resorption remains an active research area due to the lack of biomaterial platforms to support the complex structure of the bone matrix. Recently introduced, an osteoid-inspired demineralized bone paper (DBP) prepared by 20 µm thin sectioning of demineralized bovine compact bone holds promise to address this challenge as it preserves the intrinsic bony collagen structure and retains semi-transparency. Leveraging these unique features of DBP, we investigated how collagen structures modulate osteoblast and osteoclast-driven bone mineral metabolism. DBP exhibits distinct collagen structures depending on the sectioning direction, with uniaxially aligned collagen in vertical DBP (vDBP) and a concentric ring structure in transverse DBP (tDBP). Translucent DBP reveals these collagen structures and facilitates longitudinal tracking of mineral deposition and resorption under brightfield microscopy for at least 3 weeks. Genetically labeled primary osteogenic cells allow fluorescent monitoring of these cellular processes. Osteoblasts adhere and proliferate following the underlying collagen structures of DBPs, resulting in significantly higher mineral deposition in vertical DBP compared to transversal DBP. Spatiotemporal analysis reveals notably more osteoblast adhesion and faster mineral deposition in vascular regions known to contain type IV collagen and laminin than in bone regions predominantly consisting of type I collagen. Subsequent osteoclastic resorption occurs following the mineralized collagen structures, directing distinct trench and pit-type resorption. In vertical DBP, trench-type resorption occurs at an 80% frequency, whereas in transversal DBP, trench- and pit-type resorption are observed at frequencies of 35 % and 65 %, respectively. Our studies substantiate the importance of collagen structures in regulating mineral metabolism by osteogenic cells. DBP is expected to serve as an enabling biomaterial platform for studying various aspects of cellular and extracellular dynamics of bone remodeling.