Engineering articular cartilage with spatially-varying matrix composition and mechanical properties from a single stem cell population using a multi-layered hydrogel

Biomaterials. 2011 Oct;32(29):6946-52. doi: 10.1016/j.biomaterials.2011.06.014. Epub 2011 Jul 1.

Abstract

Despite significant advances in stem cell differentiation and tissue engineering, directing progenitor cells into three-dimensionally (3D) organized, native-like complex structures with spatially-varying mechanical properties and extra-cellular matrix (ECM) composition has not yet been achieved. The key innovations needed to achieve this would involve methods for directing a single stem cell population into multiple, spatially distinct phenotypes or lineages within a 3D scaffold structure. We have previously shown that specific combinations of natural and synthetic biomaterials can direct marrow-derived stem cells (MSC) into varying phenotypes of chondrocytes that resemble cells from the superficial, transitional, and deep zones of articular cartilage. In this current study, we demonstrate that layer-by-layer organization of these specific biomaterial compositions creates 3D niches that allow a single MSC population to differentiate into zone-specific chondrocytes and organize into a complex tissue structure. Our results indicate that a three-layer polyethylene glycol (PEG)-based hydrogel with chondroitin sulfate (CS) and matrix metalloproteinase-sensitive peptides (MMP-pep) incorporated into the top layer (superficial zone, PEG:CS:MMP-pep), CS incorporated into the middle layer (transitional zone, PEG:CS) and hyaluronic acid incorporated in the bottom layer (deep zone, PEG:HA), creates native-like articular cartilage with spatially-varying mechanical and biochemical properties. Specifically, collagen II levels decreased gradually from the superficial to the deep zone, while collagen X and proteoglycan levels increased, leading to an increasing gradient of compressive modulus from the superficial to the deep zone. We conclude that spatially-varying biomaterial compositions within single 3D scaffolds can stimulate efficient regeneration of multi-layered complex tissues from a single stem cell population.

Publication types

  • Evaluation Study

MeSH terms

  • Animals
  • Biocompatible Materials / chemistry*
  • Cartilage, Articular / cytology*
  • Cell Differentiation / physiology
  • Cell Proliferation
  • Cell Survival
  • Cells, Cultured
  • Collagen / metabolism
  • Compressive Strength
  • Extracellular Matrix / chemistry*
  • Glycosaminoglycans / chemistry
  • Hydrogel, Polyethylene Glycol Dimethacrylate / chemistry*
  • Materials Testing
  • Mice
  • Stem Cells / cytology
  • Stem Cells / physiology*
  • Stress, Mechanical
  • Tissue Engineering / methods*

Substances

  • Biocompatible Materials
  • Glycosaminoglycans
  • Hydrogel, Polyethylene Glycol Dimethacrylate
  • Collagen