Evaluation of Therapeutic Collagen-Based Biomaterials in the Infarcted Mouse Heart by Extracellular Matrix Targeted MALDI Imaging Mass Spectrometry

J Am Soc Mass Spectrom. 2021 Dec 1;32(12):2746-2754. doi: 10.1021/jasms.1c00189. Epub 2021 Oct 29.

Abstract

The goal of this study was to develop strategies to localize human collagen-based hydrogels within an infarcted mouse heart, as well as analyze its impact on endogenous extracellular matrix (ECM) remodeling. Collagen is a natural polymer that is abundantly used in bioengineered hydrogels because of its biocompatibility, cell permeability, and biodegradability. However, without the use of tagging techniques, collagen peptides derived from hydrogels can be difficult to differentiate from the endogenous ECM within tissues. Imaging mass spectrometry is a robust tool capable of visualizing synthetic and natural polymeric molecular structures yet is largely underutilized in the field of biomaterials outside of surface characterization. In this study, our group leveraged a recently developed matrix-assisted laser desorption/ionization imaging mass spectrometry (MALDI IMS) technique to enzymatically target collagen and other ECM peptides within the tissue microenvironment that are both endogenous and hydrogel-derived. Using a multimodal approach of fluorescence microscopy and ECM-IMS techniques, we were able to visualize and relatively quantify significantly abundant collagen peptides in an infarcted mouse heart that were localized to regions of therapeutic hydrogel injection sites. On-tissue MALDI MS/MS was used to putatively identify sites of collagen peptide hydroxyproline site occupancy, a post-translational modification that is critical in collagen triple helical stability. Additionally, the technique could putatively identify over 35 endogenously expressed ECM peptides that were expressed in hydrogel-injected mouse hearts. Our findings show evidence for the use of MALDI-IMS in assessing the therapeutic application of collagen-based biomaterials.

Keywords: MALDI; biomaterials; collagen; imaging mass spectrometry; myocardial infarction; peptides.

MeSH terms

  • Animals
  • Biocompatible Materials* / administration & dosage
  • Biocompatible Materials* / analysis
  • Biocompatible Materials* / chemistry
  • Biocompatible Materials* / pharmacokinetics
  • Collagen* / administration & dosage
  • Collagen* / analysis
  • Collagen* / chemistry
  • Collagen* / pharmacokinetics
  • Disease Models, Animal
  • Extracellular Matrix / chemistry
  • Extracellular Matrix / metabolism*
  • Female
  • Heart / diagnostic imaging
  • Histocytochemistry
  • Mice
  • Mice, Inbred C57BL
  • Molecular Imaging / methods
  • Myocardial Infarction / diagnostic imaging*
  • Myocardial Infarction / metabolism
  • Myocardium / chemistry
  • Myocardium / metabolism
  • Peptide Fragments / administration & dosage
  • Peptide Fragments / analysis
  • Peptide Fragments / chemistry
  • Peptide Fragments / pharmacokinetics
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization / methods*
  • Tissue Distribution

Substances

  • Biocompatible Materials
  • Peptide Fragments
  • Collagen