Implantation of adipose-derived mesenchymal stem cell sheets promotes axonal regeneration and restores bladder function after spinal cord injury

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Abstract

Background

Cell-based therapy using adipose-derived mesenchymal stem cells (ADSCs) is a promising treatment strategy for neurogenic bladder (NB) associated with spinal cord injury (SCI). However, therapeutic efficacy is low because of inefficient cell delivery. Cell sheets improve the efficacy of cell transplantation. Therefore, this study was conducted to investigate the therapeutic efficacy of transplanting ADSC sheets into an SCI rat model and focused on the function and pathological changes of the bladder.

Methods

ADSC sheets were prepared from adipose tissue of Sprague–Dawley (SD) rats using temperature-responsive cell culture dishes. Adult female SD rats were subjected to SCI by transection at the T10 level and administered ADSC sheets or gelatin sponge (the control group). Four and 8 weeks later, in vivo cystometrograms were obtained for voiding function assessment. Rats were sacrificed and the expression of various markers was analyzed in spinal and bladder tissues.

Results

The number of β-tubulin III-positive axons in the ADSC sheet transplantation group was higher than that in the control group. Conversely, expression of glial fibrillary acidic protein in the ADSC sheet transplantation group was lower than that in the control group. Cystometry showed impairment of the voiding function after SCI, which was improved after ADSC sheet transplantation with increased high-frequency oscillation activity. Furthermore, ADSC sheet transplantation prevented disruption of the bladder urothelium in SCI rats, thereby maintaining the intact barrier. Compared with fibrosis of the bladder wall in the control group, the ADSC sheet transplantation group had normal morphology of the bladder wall and reduced tissue fibrosis as shown by downregulation of type 1 collagen. ADSC sheet transplantation also resulted in strong upregulation of contractile smooth muscle cell (SMC) markers (α-smooth muscle actin and smoothelin) and downregulation of synthetic SMC markers (MYH10 and RBP1).

Conclusion

ADSC sheet transplantation significantly improved voiding function recovery in rats after SCI. ADSC sheet transplantation is a promising cell delivery and treatment option for NB related to SCI.

Supplementary Information

The online version contains supplementary material available at 10.1186/s13287-022-03188-1.

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Most cited references 38

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Smooth muscle cell fate and plasticity in atherosclerosis

Sima Allahverdian, Chiraz Chaâbane, Kamel Boukais … (2018)

Current knowledge suggests that intimal smooth muscle cells (SMCs) in native atherosclerotic plaque derive mainly from the medial arterial layer. During this process, SMCs undergo complex structural and functional changes giving rise to a broad spectrum of phenotypes. Classically, intimal SMCs are described as dedifferentiated/synthetic SMCs, a phenotype characterized by reduced expression of contractile proteins. Intimal SMCs are considered to have a beneficial role by contributing to the fibrous cap and thereby stabilizing atherosclerotic plaque. However, intimal SMCs can lose their properties to such an extent that they become hard to identify, contribute significantly to the foam cell population, and acquire inflammatory-like cell features. This review highlights mechanisms of SMC plasticity in different stages of native atherosclerotic plaque formation, their potential for monoclonal or oligoclonal expansion, as well as recent findings demonstrating the underestimated deleterious role of SMCs in this disease.

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Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder.

Kunyoo Shin, James Kim, John M. Lee … (2011)

Epithelial integrity in metazoan organs is maintained through the regulated proliferation and differentiation of organ-specific stem and progenitor cells. Although the epithelia of organs such as the intestine regenerate constantly and thus remain continuously proliferative, other organs, such as the mammalian urinary bladder, shift from near-quiescence to a highly proliferative state in response to epithelial injury. The cellular and molecular mechanisms underlying this injury-induced mode of regenerative response are poorly defined. Here we show in mice that the proliferative response to bacterial infection or chemical injury within the bladder is regulated by signal feedback between basal cells of the urothelium and the stromal cells that underlie them. We demonstrate that these basal cells include stem cells capable of regenerating all cell types within the urothelium, and are marked by expression of the secreted protein signal Sonic hedgehog (Shh). On injury, Shh expression in these basal cells increases and elicits increased stromal expression of Wnt protein signals, which in turn stimulate the proliferation of both urothelial and stromal cells. The heightened activity of this signal feedback circuit and the associated increase in cell proliferation appear to be required for restoration of urothelial function and, in the case of bacterial injury, may help clear and prevent further spread of infection. Our findings provide a conceptual framework for injury-induced epithelial regeneration in endodermal organs, and may provide a basis for understanding the roles of signalling pathways in cancer growth and metastasis. ©2011 Macmillan Publishers Limited. All rights reserved

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Modern Medical Management of Spinal Cord Injury

Michael Karsy, Gregory Hawryluk (2019)

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Author and article information

Contributors

Qiang Fu: jamesqfu@126.com

Ying Wang: sdzbbswangying@alumni.sjtu.edu.cn

Journal

Journal ID (nlm-ta): Stem Cell Res Ther

Journal ID (iso-abbrev): Stem Cell Res Ther

Title: Stem Cell Research & Therapy

Publisher: BioMed Central (London )

ISSN (Electronic): 1757-6512

Publication date (Electronic): 12 October 2022

Publication date PMC-release: 12 October 2022

Publication date Collection: 2022

Volume: 13

Electronic Location Identifier: 503

Affiliations

[1 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, Department of Urology, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai Eastern Institute of Urologic Reconstruction, , Shanghai Jiao Tong University, ; Shanghai, China

[2 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, Key Laboratory for Thin Film and Micro Fabrication of the Ministry of Education, School of Sensing Science and Engineering, School of Electronic Information and Electrical Engineering, , Shanghai Jiao Tong University, ; Shanghai, China

[3 ]GRID grid.241167.7, ISNI 0000 0001 2185 3318, Wake Forest Institute for Regenerative Medicine, ; Winston Salem, NC USA

Article

Publisher ID: 3188

DOI: 10.1186/s13287-022-03188-1

PMC ID: 9558366

PubMed ID: 36224621

SO-VID: d4e28040-ae5e-441a-ae0e-40eb6db264b3

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 10 April 2022

Date accepted : 30 September 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 82100714

Award ID: 82170694

Award Recipient : Qiang Fu Ying Wang

Custom metadata

ScienceOpen disciplines: Molecular medicine

Keywords: adipose-derived mesenchymal stem cells (adscs),spinal cord injury (sci),cell sheets,cell-based therapy,neurogenic bladder (nb)

Data availability:

ScienceOpen disciplines: Molecular medicine

Keywords: adipose-derived mesenchymal stem cells (adscs), spinal cord injury (sci), cell sheets, cell-based therapy, neurogenic bladder (nb)

Implantation of adipose-derived mesenchymal stem cell sheets promotes axonal regeneration and restores bladder function after spinal cord injury

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Abstract

Background

Methods

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Conclusion

Supplementary Information

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cGMP: Generators, Effectors and Therapeutic Implications Conference

Most cited references 38

Smooth muscle cell fate and plasticity in atherosclerosis

Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder.

Modern Medical Management of Spinal Cord Injury

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