A bioartificial and vasculomorphic bone matrix-based organoid mimicking microanatomy of flat and short bones.

bone remodeling mesenchymal stromal cell microtopography organoid osteoporosis polylevolactic acid scaffold

Journal

Journal of biomedical materials research. Part B, Applied biomaterials
ISSN: 1552-4981
Titre abrégé: J Biomed Mater Res B Appl Biomater
Pays: United States
ID NLM: 101234238

Informations de publication

Date de publication:
29 Oct 2023
Historique:
revised: 08 08 2023
received: 03 04 2023
accepted: 07 09 2023
medline: 29 10 2023
pubmed: 29 10 2023
entrez: 29 10 2023
Statut: aheadofprint

Résumé

We engineered an in vitro model of bioartificial 3D bone organoid consistent with an anatomical and vascular microenvironment common to mammalian flat and short bones. To achieve this, we chose the decellularized-decalcified matrix of the adult male rat scapula, implemented with the reconstruction of its intrinsic vessels, obtained through an original intravascular perfusion with polylevolactic (PLLA), followed by coating of the PLLA-fabricated vascularization with rat tail collagen. As a result, the 3D bone and vascular geometry of the native bone cortical and cancellous compartments was reproduced, and the rat tail collagen-PLLA biomaterial could in vitro act as a surrogate of the perivascular extracellular matrix (ECM) around the wall of the biomaterial-reconstituted cancellous vessels. As a proof-of-concept of cell compatibility and site-dependent osteoinductive properties of this bioartificial 3D construct, we show that it in vitro leads to a time-dependent microtopographic positioning of rat mesenchymal stromal cells (MSCs), initiating an osteogenic fate in relation to the bone compartment. In addition, coating of PLLA-reconstructed vessels with rat tail collagen favored perivascular attachment and survival of MSC-like cells (mouse embryonic fibroblasts), confirming its potentiality as a perivascular stroma for triggering competence of seeded MSCs. Finally, in vivo radiographic topography of bone lesions in the human jaw and foot tarsus of subjects with primary osteoporosis revealed selective bone cortical versus cancellous involvement, suggesting usefulness of a human 3D bone organoid engineered with the same principles of our rat organoid, to in vitro investigate compartment-dependent activities of human MSC in flat and short bones under experimental osteoporotic challenge. We conclude that our 3D bioartificial construct offers a reliable replica of flat and short bones microanatomy, and promises to help in building a compartment-dependent mechanistic perspective of bone remodeling, including the microtopographic dysregulation of osteoporosis.

Identifiants

pubmed: 37898921
doi: 10.1002/jbm.b.35329
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : FIL UNIPR 2020 2022
Organisme : HORIZON 2020 825745
Organisme : SISMA RIPOPOLAMENTO ER 2019

Informations de copyright

© 2023 The Authors. Journal of Biomedical Materials Research Part B: Applied Biomaterials published by Wiley Periodicals LLC.

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Auteurs

Roberto Toni (R)

ISSMC, CNR, Faenza, Italy.
Department of Medicine, Division of Endocrinology, Diabetes, and Metabolism, Tufts Medical Center-Tufts University School of Medicine, Boston, Massachusetts, USA.
Academy of Sciences of the Institute of Bologna, Section IV-Medical Sciences, Bologna, Italy.
Endocrinology, Diabetes, and Nutrition Disorders Outpatient Clinic-OSTEONET (Osteoporosis, Nutrition, Endocrinology, and Innovative Therapies) and Odontostomatology Units, Galliera Medical Center, San Venanzio di Galliera (BO), Italy.

Fulvio Barbaro (F)

Department of Medicine and Surgery-DIMEC, Unit of Biomedical, Biotechnological and Translational Sciences (S.BI.BI.T.), Laboratory of Regenerative Morphology and Bioartificial Structures (Re.Mo.Bio.S.), and Museum and Historical Library of Biomedicine-BIOMED, University of Parma, Parma, Italy.

Giusy Di Conza (G)

Department of Medicine and Surgery-DIMEC, Unit of Biomedical, Biotechnological and Translational Sciences (S.BI.BI.T.), Laboratory of Regenerative Morphology and Bioartificial Structures (Re.Mo.Bio.S.), and Museum and Historical Library of Biomedicine-BIOMED, University of Parma, Parma, Italy.

Nicoletta Zini (N)

CNR Institute of Molecular Genetics "Luigi Luca Cavalli-Sforza", Unit of Bologna, Bologna, Italy.
IRCCS Istituto Ortopedico Rizzoli, Bologna, Italy.

Giulia Remaggi (G)

Food and Drug Department, University of Parma, Parma, Italy.

Lisa Elviri (L)

Food and Drug Department, University of Parma, Parma, Italy.

Giulia Spaletta (G)

Department of Statistical Sciences, University of Bologna, Bologna, Italy.

Enrico Quarantini (E)

Endocrinology, Diabetes, and Nutrition Disorders Outpatient Clinic-OSTEONET (Osteoporosis, Nutrition, Endocrinology, and Innovative Therapies) and Odontostomatology Units, Galliera Medical Center, San Venanzio di Galliera (BO), Italy.

Marco Quarantini (M)

Endocrinology, Diabetes, and Nutrition Disorders Outpatient Clinic-OSTEONET (Osteoporosis, Nutrition, Endocrinology, and Innovative Therapies) and Odontostomatology Units, Galliera Medical Center, San Venanzio di Galliera (BO), Italy.

Salvatore Mosca (S)

Course on Disorders of the Locomotor System, Fellow Program in Orthopaedics and Traumatology, University Vita-Salute San Raffaele, Milan, Italy.

Silvio Caravelli (S)

II Clinic of Orthopedic and Traumatology, IRCCS Istituto Ortopedico Rizzoli, Bologna, Italy.

Massimiliano Mosca (M)

II Clinic of Orthopedic and Traumatology, IRCCS Istituto Ortopedico Rizzoli, Bologna, Italy.

Francesca Ravanetti (F)

Department of Veterinary Medical Sciences, Section of Anatomy, University of Parma, Parma, Italy.

Simone Sprio (S)

ISSMC, CNR, Faenza, Italy.

Anna Tampieri (A)

ISSMC, CNR, Faenza, Italy.

Classifications MeSH