Magnetic resonance contrast and biological effects of intracellular superparamagnetic iron oxides on human mesenchymal stem cells with long-term culture and hypoxic exposure

Rosenberg, Jens T.; Sellgren, Katelyn L.; Sachi-Kocher, Afi; Bejarano, Fabian Calixto; Baird, Michelle A.; Davidson, Michael W.; Ma, Teng; Grant, Samuel C.

doi:10.1016/j.jcyt.2012.10.013

Cited by 25 publications

(35 citation statements)

References 80 publications

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“…Notably, a progressive decrease of intracellular Fe 3 O 4 NPs over increasing culture time was observed. As several reports have suggested, using different IONPs at various concentrations on BM‐MSCs cultured for 7‐14 days (Harrison et al, ; Mohanty et al, ; Rosenberg et al, ), we also believe that this apparent dilution effect of IONPs is to be attributed to cell division.…”

Section: Discussionsupporting

confidence: 60%

“…To date, most in vitro Fe 3 O 4 NP toxicity information was derived from studies carried out on immortalized or tumorigenic cells (Coccini, Caloni, Ramírez Cando, & De Simone, ; Guadagnini, Moreau, Hussain, Marano, & Boland, ; Mahmoudi, Hofmann, Rutishauser, & Fink, ; Malvindi et al, ; Sanganeria, Sachar, et al, ). Recent studies have started to apply MSCs for Fe 3 O 4 NP toxicity evaluation (in terms of cytotoxicity, MSC differentiation capacity and iron uptake), which mostly derive from BM (Hachani et al, ; Harrison et al, ; Rosenberg et al, ), few from UC tissue (Dulinska‐Molak et al, ; Hu et al, ; Periasamy, Athinarayanan, Alhazmi, Alatiah, & Alshatwi, ) and only one from CL‐MSC (Sanganeria, Chandra, Bahadur, & Khanna, ).…”

Section: Introductionmentioning

confidence: 99%

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In vitro toxicity screening of magnetite nanoparticles by applying mesenchymal stem cells derived from human umbilical cord lining

Coccini

Simone

Roccio

et al. 2019

J of Applied Toxicology

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Despite the growing interest in nanoparticles (NPs), their toxicity has not yet been defined and the development of new strategies and predictive models are required. Human stem cells (SCs) offer a promising and innovative cell-based model. Among SCs, mesenchymal SCs (MSCs) derived from cord lining membrane (CL) may represent a new species-specific tool for establishing efficient platforms for primary screening and toxicity/safety testing of NPs. Superparamagnetic iron oxide NPs, including magnetite (Fe 3 O 4 NPs), have aroused great public health and scientific concerns despite their extensive uses. In this study, CL-MSCs were characterized and applied for in vitro toxicity screening of Fe 3 O 4 NPs. Cytotoxicity, internalization/uptake, differentiation and proliferative capacity were evaluated after exposure to different Fe 3 O 4 NP concentrations. Data were compared with those obtained from bone marrow (BM)-MSCs. We observed, at early passages (P3), that: (1) cytotoxicity occurred at 10 μg/mL in CL-MSCs and 100 μg/mL in BM-MSCs (no differences in toxicity, between CL-and BM-MSCs, were observed at higher dosage, 100-300 μg/mL); (2) cell density decrease and monolayer features loss were affected at ≥50 μg/mL in CL-MSCs only; and (3) NP uptake was concentration-dependent in both MSCs. After 100 μg/mL Fe 3 O 4 NP exposures, the capacity of proliferation was decreased (P5-P9) in CL-MSCs without morphology alteration. Moreover, a progressive decrease of intracellular Fe 3 O 4 NPs was observed over culture time. Antigen surface expression and multilineage differentiation were not influenced. These findings suggest that CL-MSCs could be used as a reliable cell-based model for Fe 3 O 4 NP toxicity screening evaluation and support the use of this approach for improving the confidence degree on the safety of NPs to predict health outcomes. KEYWORDS bone marrow, environmental and occupational exposure, human cell model, in vitro, mesenchymal stem cells, risk assessment, toxicity, umbilical cord lining

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Section: Discussionsupporting

confidence: 60%

Section: Introductionmentioning

confidence: 99%

In vitro toxicity screening of magnetite nanoparticles by applying mesenchymal stem cells derived from human umbilical cord lining

Coccini

Simone

Roccio

et al. 2019

J of Applied Toxicology

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“…To analyze MRI detectability, MPIO‐labeled EB‐NPCs before and after cryopreservation were immobilized in agarose gels to provide a controlled tissue mimicking phantom for which T 2 and T 2 * relaxations were correlated with the initial MPIO exposure . The in vitro MRI measurements provide a controllable method of modeling contrast effects, which are critical to monitor the transplanted cells in vivo.…”

Section: Discussionmentioning

confidence: 99%

Cryopreservation of embryonic stem cell‐derived multicellular neural aggregates labeled with micron‐sized particles of iron oxide for magnetic resonance imaging

Yan

Sart

Bejarano

et al. 2015

Biotechnology Progress

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Magnetic resonance imaging (MRI) provides an effective approach to track labeled pluripotent stem cell (PSC)-derived neural progenitor cells (NPCs) for neurological disorder treatments after cell labeling with a contrast agent, such as an iron oxide derivative. Cryopreservation of pre-labeled neural cells, especially in three-dimensional (3D) structure, can provide a uniform cell population and preserve the stem cell niche for the subsequent applications. In this study, the effects of cryopreservation on PSC-derived multicellular NPC aggregates labeled with micron-sized particles of iron oxide (MPIO) were investigated. These NPC aggregates were labeled prior to cryopreservation because labeling thawed cells can be limited by inefficient intracellular uptake, variations in labeling efficiency, and increased culture time before use, minimizing their translation to clinical settings. The results indicated that intracellular MPIO incorporation was retained after cryopreservation (70-80% labeling efficiency), and MPIO labeling had little adverse effects on cell recovery, proliferation, cytotoxicity and neural lineage commitment post-cryopreservation. MRI analysis showed comparable detectability for the MPIO-labeled cells before and after cryopreservation indicated by T2 and T2* relaxation rates. Cryopreserving MPIO-labeled 3D multicellular NPC aggregates can be applied in in vivo cell tracking studies and lead to more rapid translation from preservation to clinical implementation.

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“…To answer this question, studies been performed using superparamagnetic iron oxides (SPIO) to mark hMSCs-UC in combination with an MRI technique 14; however, the MRI signal becomes weaker with the progressive differentiation of hMSCs-UC in the target tissue in the animal model, and therefore this method is not suitable for long-term observation. A recent study showed that higher dose SPIO labeling is stable for long-term MRI detection, but the labeling may limit the multi-lineage potential of hMSCs and affect their survival under serum and oxygen withdrawal 24. The daily clinical usage of gadolinium (Gd) based contrast agents in magnetic resonance imaging is limited because of its nephrogenic toxicity 25.…”

Section: Discussionmentioning

confidence: 99%

Localization of Human Mesenchymal Stem Cells from Umbilical Cord Blood and Their Role in Repair of Diabetic Foot Ulcers in Rats

et al. 2014

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The aim of this study is to explore the localization of human mesenchymal stem cells from umbilical cord matrix (hMSCs-UC) and the role of these cells in the repair of foot ulcerate tissue in diabetic foot ulcers in rats. A diabetic rat model was established by administering Streptozotocin. Diabetic foot ulceration was defined as non-healing or delayed-healing of empyrosis on the dorsal hind foot after 14 weeks. hMSCs-UC were delivered through the left femoral artery. We evaluated the localization of hMSCs-UC and their role in tissue repair in diabetic foot ulcers by histological analysis, PCR, and immunohistochemical staining. A model for diabetes was established in 54 out of 60 rats (90% success rate) and 27 of these rats were treated with hMSCs-UC. The area of ulceration was significantly and progressively reduced at 7 and 14 days following treatment with hMSCs-UC. This gross observation was strongly supported by the histological changes, including newly developed blood vessels and proliferation of inflammatory cells at 3 days post-treatment, significant increase in granulation tissue at 7 days post-treatment and squamous epithelium or stratified squamous epithelium at 14 days post-treatment. Importantly, human leukocyte antigen type-I (HLA-1) was confirmed in ulcerated tissue by RT-PCR. The expression of cytokeratin 19 was significantly increased in diabetic model rats, with no detectable change in cytokeratin 10. Additionally, both collagens I and III increased in model rats treated with hMSCs-UC, but the ratio of collagen I/III was less significant in treated rats compared with control rats. These results suggest that hMSCs-UC specifically localize to the target ulcerated tissue and may promote the epithelialization of ulcerated tissue by stimulating the release of cytokeratin 19 from keratinocytes and extracellular matrix formation.

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Magnetic resonance contrast and biological effects of intracellular superparamagnetic iron oxides on human mesenchymal stem cells with long-term culture and hypoxic exposure

Cited by 25 publications

References 80 publications

In vitro toxicity screening of magnetite nanoparticles by applying mesenchymal stem cells derived from human umbilical cord lining

In vitro toxicity screening of magnetite nanoparticles by applying mesenchymal stem cells derived from human umbilical cord lining

Cryopreservation of embryonic stem cell‐derived multicellular neural aggregates labeled with micron‐sized particles of iron oxide for magnetic resonance imaging

Localization of Human Mesenchymal Stem Cells from Umbilical Cord Blood and Their Role in Repair of Diabetic Foot Ulcers in Rats

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