Therapeutic reversal of radiotherapy injury to pro-fibrotic dysfunctional fibroblasts in vitro using adipose-derived stem cells

Journal article


Shukla, Lipi, Luwor, Rodney B., Ritchie, Matthew E, Akbarzadeh, Shiva, Zhu, Hong-Jian, Morrison, Wayne, Karnezis, Tara and Shayan, Ramin. (2020). Therapeutic reversal of radiotherapy injury to pro-fibrotic dysfunctional fibroblasts in vitro using adipose-derived stem cells. Plastic and Reconstructive Surgery - Global Open. 8(3), p. Article e2706. https://doi.org/10.1097/GOX.0000000000002706
AuthorsShukla, Lipi, Luwor, Rodney B., Ritchie, Matthew E, Akbarzadeh, Shiva, Zhu, Hong-Jian, Morrison, Wayne, Karnezis, Tara and Shayan, Ramin
Abstract

Background:
Cancer patients often require radiotherapy (RTx) to enhance their survival. Unfortunately, RTx also damages nearby healthy non-cancer tissues, leading to progressive fibrotic soft-tissue injury, consisting of pain, contracture, tissue-breakdown, infection, and lymphoedema. Mechanisms underlying the clinically observed ability of fat grafting to ameliorate some of these effects, however, are poorly understood. It was hypothesized that RTx significantly alters fibroblast cell function and the paracrine secretome of adipose-derived stem cells (ADSC) may mitigate these changes.

Methods:
To investigate cellular changes resulting in the fibrotic side-effects of RTx, cultured normal human dermal fibroblasts (NHDF) were irradiated (10Gy), then studied using functional assays that reflect key fibroblast functions, and compared with unirradiated controls. RNA-Seq and targeted microarrays (with specific examination of TGFβ) were performed to elucidate altered gene pathways. Finally, conditioned-media from ADSC was used to treat irradiated fibroblasts and model fat graft surgery.

Results:
RTx altered NHDF morphology, with cellular functional changes reflecting transition into a more invasive phenotype: increased migration, adhesion, contractility, and disordered invasion. Changes in genes regulating collagen and MMP homeostasis and cell-cycle progression were also detected. However, TGFβ was not identified as a key intracellular regulator of the fibroblast response. Finally, treatment with ADSC-conditioned media reversed the RTx-induced hypermigratory state of NHDF.

Conclusions:
Our findings regarding cellular and molecular changes in irradiated fibroblasts help explain clinical manifestations of debilitating RTx-induced fibrosis. ADSC-secretome-mediated reversal indicated that these constituents may be used to combat the devastating side-effects of excessive unwanted fibrosis in RTx and other human fibrotic diseases.

Year2020
JournalPlastic and Reconstructive Surgery - Global Open
Journal citation8 (3), p. Article e2706
PublisherLippincott Williams & Wilkins
ISSN2169-7574
Digital Object Identifier (DOI)https://doi.org/10.1097/GOX.0000000000002706
PubMed ID32537359
Scopus EID2-s2.0-85104011425
PubMed Central IDPMC7253248
Open accessPublished as ‘gold’ (paid) open access
Page range1-9
Publisher's version
License
File Access Level
Open
Output statusPublished
Publication dates
OnlineMar 2020
Publication process dates
Accepted27 Jan 2020
Deposited15 Nov 2023
Permalink -

https://acuresearchbank.acu.edu.au/item/8zz18/therapeutic-reversal-of-radiotherapy-injury-to-pro-fibrotic-dysfunctional-fibroblasts-in-vitro-using-adipose-derived-stem-cells

Download files


Publisher's version
OA_Shukla_2020_Therapeutic_reversal_of_radiotherapy_injury_to.pdf
License: CC BY-NC-ND 4.0
File access level: Open

  • 46
    total views
  • 22
    total downloads
  • 3
    views this month
  • 0
    downloads this month
These values are for the period from 19th October 2020, when this repository was created.

Export as

Related outputs

Liver specification of human iPSC-derived endothelial cells transplanted into mouse liver
Yap, Kiryu K., Schröder, Jan, Gerrand, Yi-Wen, Dobric, Aleksandar, Kong, Anne M, Fox, Adrian M., Knowles, Brett, Banting, Simon W., Elefanty, Andrew G., Stanley, Eduoard G., Yeoh, George C., Lockwood, Glen P., Cogger, Victoria C., Morrison, Wayne, Polo, Jose M. and Mitchell, Geraldine. (2024). Liver specification of human iPSC-derived endothelial cells transplanted into mouse liver. JHEP Reports. 6(5), pp. 1-18. https://doi.org/10.1016/j.jhepr.2024.101023
Basic skin flaps and blood supply
Morrison, Edwin and Morrison, Wayne A. J.. (2022). Basic skin flaps and blood supply. In In Bulstrode, Neil W., Cugno, Sabrina and Mehrara, Babak J. (Ed.). Plastic surgery - Principles and practice pp. 15-26 Elsevier Inc.. https://doi.org/10.1016/B978-0-323-65381-7.00002-2
Digital replantation and thumb reconstruction
Morrison, Wayne A. J., Farhadieh, Rostam D. and Perotti, Olivia M.. (2022). Digital replantation and thumb reconstruction. In In Bulstrode, Neil W., Cugno, Sabrina and Mehrara, Babak J. (Ed.). Plastic surgery - Principles and practice pp. 774-792 Elsevier Inc.. https://doi.org/10.1016/B978-0-323-65381-7.00050-2
Engineering transplantable human lymphatic and blood capillary networks in a porous scaffold
Kong, Anne M., Lim, Shiang Y., Palmer, Jason A., Rixon, Amanda, Gerrand, Yi-Wen, Yap, Kiryu K., Morrison, Wayne A. and Mitchell, Geraldine M.. (2022). Engineering transplantable human lymphatic and blood capillary networks in a porous scaffold. Journal of Tissue Engineering. 13, pp. 1-21. https://doi.org/10.1177/20417314221140979
Pharyngeal Reconstruction
Farhadieh, Rostam D., Sud, Ajay R., Morrison, Edwin and Morrison, Wayne. (2021). Pharyngeal Reconstruction. In Plastic Surgery - Principles and Practice pp. 364-376 Elsevier. https://doi.org/10.1016/B978-0-323-65381-7.00026-5
Australian and New Zealand contribution to Plastic Surgery
Yousef, Justin and Morrison, Wayne. (2021). Australian and New Zealand contribution to Plastic Surgery. ANZ Journal of Surgery. 91(7-8), pp. 1428-1434. https://doi.org/10.1111/ans.16650
Liver sinusoidal endothelial cells promote the differentiation and survival of mouse vascularised hepatobiliary organoids
Yap, Kiryu K., Gerrand, Yi-Wen, Dingle, Aaron M., Yeoh, George C., Morrison, Wayne A. and Mitchell, Geraldine M.. (2020). Liver sinusoidal endothelial cells promote the differentiation and survival of mouse vascularised hepatobiliary organoids. Biomaterials. 251, p. 120091. https://doi.org/10.1016/j.biomaterials.2020.120091
Scaffolds for dermal tissue engineering
Debels, Heidi and Morrison, Wayne. (2019). Scaffolds for dermal tissue engineering. In Handbook of tissue engineering scaffolds : Volume two pp. 147-172 Elsevier Ltd. https://doi.org/10.1016/B978-0-08-102561-1.00006-3
Selenium nanoparticles as anti-infective implant coatings for trauma orthopedics against methicillin-resistant Staphylococcus aureus and epidermidis : In vitro and in vivo assessment
Tran, Phong A., O'Brien-Simpson, Neil, Palmer, Jason A., Bock, Nathalie, Reynolds, Eric C., Webster, Thomas J., Deva, Anand, Morrison, Wayne A. and O'Connor, Andrea J.. (2019). Selenium nanoparticles as anti-infective implant coatings for trauma orthopedics against methicillin-resistant Staphylococcus aureus and epidermidis : In vitro and in vivo assessment. International Journal of Nanomedicine. 14, pp. 4613-4624. https://doi.org/10.2147/IJN.S197737
Vascular pedicle and microchannels : Simple methods toward effective in vivo vascularization of 3D scaffolds
Rnjak-Kovacina, Jelena, Gerrand, Yi-wen, Wray, Lindsay S., Tan, Beryl, Joukhdar, Habib, Kaplan, David L., Morrison, Wayne A. and Mitchell, Geraldine M.. (2019). Vascular pedicle and microchannels : Simple methods toward effective in vivo vascularization of 3D scaffolds. Advanced Healthcare Materials. 8(24), p. 1901106. https://doi.org/10.1002/adhm.201901106
Bio-engineering a tissue flap utilizing a porous scaffold incorporating a human induced pluripotent stem cell-derived endothelial cell capillary network connected to a vascular pedicle
Kong, Anne M., Yap, Kiryu K., Lim, Shiang Y., Marre, Diego, Pébay, Alice, Gerrand, Yi-wen, Lees, Jarmon G., Palmer, Jason A., Morrison, Wayne A. and Mitchell, Geraldine M.. (2019). Bio-engineering a tissue flap utilizing a porous scaffold incorporating a human induced pluripotent stem cell-derived endothelial cell capillary network connected to a vascular pedicle. Acta Biomaterialia. 94, pp. 281-294. https://doi.org/10.1016/j.actbio.2019.05.067
Melatonin promotes survival of nonvascularized fat grafts and enhances the viability and migration of human adipose-derived stem cells via down-regulation of acute inflammatory cytokines
Tan, Shaun S., Zhan, Weiqing, Poon, Christopher J., Han, Xiaolian, Marre, Diego, Boodhun, Sholeh, Palmer, Jason A., Mitchell, Geraldine M. and Morrison, Wayne A.. (2018). Melatonin promotes survival of nonvascularized fat grafts and enhances the viability and migration of human adipose-derived stem cells via down-regulation of acute inflammatory cytokines. Journal of Tissue Engineering and Regenerative Medicine. 12(2), pp. 382-392. https://doi.org/10.1002/term.2463
The Vascularised Chamber as an In Vivo Bioreactor
Kiryu K. Yap, George Yeoh, Wayne Morrison and Geraldine Mitchell. (2018). The Vascularised Chamber as an In Vivo Bioreactor. Trends in Biotechnology. 36(10), pp. 1011-1024. https://doi.org/10.1016/j.tibtech.2018.05.009
Fate of Free Fat Grafts with or without Adipogenic Adjuncts to Enhance Graft Outcomes
Howard Ho Fung Tang, Xiao-Lian Han, Heidi Debels, Beryl Tan, Jason Palmer, Christopher Poon, Keren Abberton and Wayne Morrison. (2018). Fate of Free Fat Grafts with or without Adipogenic Adjuncts to Enhance Graft Outcomes. Plastic and Reconstructive Surgery. 142(4), pp. 939-950. https://doi.org/10.1097/PRS.0000000000004739
Characterization of isolated liver sinusoidal endothelial cells for liver bioengineering
Aaron M. Dingle, Kiryu K. Yap, Yi-Wen Gerrand, Carolyn Taylor, Efthimia Keramidaris, Zerina Lokmic, A.M. Kong, H.L. Peters, Wayne Morrison and Geraldine Mitchell. (2018). Characterization of isolated liver sinusoidal endothelial cells for liver bioengineering. Angiogenesis. 21(3), pp. 581-597. https://doi.org/10.1007/s10456-018-9610-0
Biocompatible porous polyester-ether hydrogel scaffolds with cross-linker mediated biodegradation and mechanical properties for tissue augmentation
Berkay Ozcelik, Jason Palmer, Katharina Ladewig, Paula Facal Marina, Geoffrey W. Stevens, Keren Abberton, Wayne Morrison, Anton Blencowe and Greg G. Qiao. (2018). Biocompatible porous polyester-ether hydrogel scaffolds with cross-linker mediated biodegradation and mechanical properties for tissue augmentation. Polymers. 10(2), pp. 1-19. https://doi.org/10.3390/polym10020179
A novel microsurgical rodent model for the transplantation of engineered cardiac muscle flap
Richard Tee, Wayne Morrison and Rodney J Dilley. (2018). A novel microsurgical rodent model for the transplantation of engineered cardiac muscle flap. Microsurgery. 38(5), pp. 544-552. https://doi.org/10.1002/micr.30325
Thiol surface functionalization via continuous phase plasma polymerization of allyl mercaptan, with subsequent maleimide-linked conjugation of collagen
Stynes, Gil D., Gengenbach, Thomas R., Kiroff, George K., Morrison, Wayne A. and Kirkland, Mark A.. (2017). Thiol surface functionalization via continuous phase plasma polymerization of allyl mercaptan, with subsequent maleimide-linked conjugation of collagen. Journal of Biomedical Materials Research Part A. 105(7), pp. 1940-1948. https://doi.org/10.1002/jbm.a.36064
Surface-bound collagen 4 is significantly more stable than collagen 1
Stynes, Gil D., Kiroff, George K., Page, Richard S., Morrison, Wayne A. and Kirkland, Mark A.. (2017). Surface-bound collagen 4 is significantly more stable than collagen 1. Journal of Biomedical Materials Research Part A. 105(5), pp. 1364-1373. https://doi.org/10.1002/jbm.a.36019
Collagen immunoassay as a method to optimise surface functionalisation
Stynes, Gil, Kiroff, George, Morrison, Wayne and Kirkland, Mark. (2017). Collagen immunoassay as a method to optimise surface functionalisation. Plasma Processes and Polymers. 14(9), p. 1600213. https://doi.org/10.1002/ppap.201600213
Melatonin protects human adipose-derived stem cells from oxidative stress and cell death
Tan, Shaun S., Han, Xiaolian, Sivakumaran, Priyadharshini, Lim, Shiang Y. and Morrison, Wayne A.. (2016). Melatonin protects human adipose-derived stem cells from oxidative stress and cell death. Archives of Plastic Surgery. 43(3), pp. 237-241. https://doi.org/10.5999/aps.2016.43.3.237
Cardiac repair with a novel population of mesenchymal stem cells resident in the human heart
Zhang, Yuan, Sivakumaran, Priyadharshini, Newcomb, Andrew, Hernandez, Damian, Harris, Nicole, Khanabdali, Ramin, Liu, Guei-Sheung, Kelly, Darren, Pebay, Alice, Hewitt, Alex, Boyle, Andrew, Harvey, Richard, Morrison, Wayne, Elliot, David, Dusting, Gregory and Lim, Shiang. (2015). Cardiac repair with a novel population of mesenchymal stem cells resident in the human heart. Stem Cells. 33(10), pp. 3100 - 3113. https://doi.org/10.1002/stem.2101
Funding analysis of bilateral autologous free-flap breast reconstructions in Australia
Sinha, Shiba, Ruskin, Olivia, McCombe, David B., Morrison, Wayne and Webb, Angela. (2015). Funding analysis of bilateral autologous free-flap breast reconstructions in Australia. Journal of Plastic, Reconstructive and Aesthetic Surgery. 68(8), pp. 1120 - 1126. https://doi.org/10.1016/j.bjps.2015.04.004
Macrophage phenotype in response to implanted synthetic scaffolds : An immunohistochemical study in the rat
Palmer, Jason, Mitchell, Geraldine M., Morrison, Wayne and Abberton, Keren. (2014). Macrophage phenotype in response to implanted synthetic scaffolds : An immunohistochemical study in the rat. Cells Tissues Organs. 199(2-3), pp. 169 - 183. https://doi.org/10.1159/000363693
Highly porous and mechanically robust polyester poly(ethylene glycol) sponges as implantable scaffolds
Ozcelik, Berkay, Blencowe, Anton, Palmer, Jason, Ladewig, Katharina, Stevens, Geoffrey, Abberton, Keren, Morrison, Wayne and Qiao, Greg. (2014). Highly porous and mechanically robust polyester poly(ethylene glycol) sponges as implantable scaffolds. Acta Biomaterialia. 10(6), pp. 2769 - 2780. https://doi.org/10.1016/j.actbio.2014.02.019
The adipogenic potential of various extracellular matrices under the influence of an angiogenic growth factor combination in a mouse tissue engineering chamber
Ting, Adrian, Craft, Randall, Palmer, Jason, Gerrand, Yi-Wen, Penington, Anthony, Morrison, Wayne and Mitchell, Geraldine. (2014). The adipogenic potential of various extracellular matrices under the influence of an angiogenic growth factor combination in a mouse tissue engineering chamber. Acta Biomaterialia. 10(5), pp. 1907 - 1918. https://doi.org/10.1016/j.actbio.2013.11.019
Macrophages play a key role in angiogenesis and adipogenesis in a mouse tissue engineering model
Debels, Heidi, Galea, Laurence, Han, Xiao, Palmer, Jason, van Rooijen, Nico, Morrison, Wayne and Abberton, Keren. (2013). Macrophages play a key role in angiogenesis and adipogenesis in a mouse tissue engineering model. Tissue Engineering Part A. https://doi.org/10.1089/ten.tea.2013.0071
Enhanced liver progenitor cell survival and differentiation in vivo by spheroid implantation in a vascularized tissue engineering chamber
Yap, Kiryu, Dingle, Aaron, Palmer, Jason, Dillon, Raminder, Lokmic, Zerina, Penington, Anthony, Yeoh, George, Morrison, Wayne and Mitchell, Geraldine. (2013). Enhanced liver progenitor cell survival and differentiation in vivo by spheroid implantation in a vascularized tissue engineering chamber. Biomaterials. 34(16), pp. 3992 - 4001. https://doi.org/10.1016/j.biomaterials.2013.02.011
An adipoinductive role of inflammation in adipose tissue engineering : key factors in the early development of engineered soft tissues
Lilja, Heidi, Morrison, Wayne, Han, Xiao-Lian, Palmer, Jason, Taylor, Caroline, Tee, Richard, Moller, Andreas, Thompson, Erik and Abberton, Keren. (2013). An adipoinductive role of inflammation in adipose tissue engineering : key factors in the early development of engineered soft tissues. Stem Cells and Development. https://doi.org/10.1089/scd.2012.0451
Preparation of an adipogenic hydrogel from subcutaneous adipose tissue
Poon, Christopher, Pereira E Cotta, Maria, Sinha, Shiba, Palmer, Jason, Woods, Alan, Morrison, Wayne and Abberton, Keren. (2013). Preparation of an adipogenic hydrogel from subcutaneous adipose tissue. Acta Biomaterialia. https://doi.org/10.1016/j.actbio.2012.11.003
Adipose-derived stem cells promote angiogenesis and tissue formation for In Vivo tissue engineering
Matsuda, Ken, Falkenberg, Katrina, Woods, Alan, Choi, Yu, Morrison, Wayne and Dilley, Rodney. (2013). Adipose-derived stem cells promote angiogenesis and tissue formation for In Vivo tissue engineering. Tissue Engineering Part A. https://doi.org/10.1089/ten.tea.2012.0391
A prevascularized tissue engineering chamber supports growth and function of islets and progenitor cells in diabetic mice
Forster, Natasha, Penington, Anthony, Hardikar, Anandwardhan, Palmer, Jason, Hussey, Allan, Tai, John, Morrison, Wayne and Feeney, Sandra. (2011). A prevascularized tissue engineering chamber supports growth and function of islets and progenitor cells in diabetic mice. Islets. 3(5), pp. 271 - 283. https://doi.org/10.4161/isl.3.5.15942
Intrinsics and dynamics of fat grafts: An in vitro study
Stillaert, Filip B., Abberton, Keren, Keramidaris, Efthimia, Thompson, Erik, Blondeel, Phillip Nicholas V. and Morrison, Wayne. (2010). Intrinsics and dynamics of fat grafts: An in vitro study. Plastic and Reconstructive Surgery. 126(4), pp. 1155 - 1162. https://doi.org/10.1097/PRS.0b013e3181ebe224
Vascularized tissue engineering mouse chamber model supports thymopoiesis of ectopic thymus tissue grafts
Seach, Natalie, Mattesich, Monika, Abberton, Keren, Matsuda, Ken, Tilkorn, Daniel J., Rophael, John, Boyd, Richard L. and Morrison, Wayne. (2010). Vascularized tissue engineering mouse chamber model supports thymopoiesis of ectopic thymus tissue grafts. Tissue Engineering Part C: Methods. 16(3), pp. 543 - 551. https://doi.org/10.1089/ten.tec.2009.0135
Engineering cardiac tissue in vivo from human adipose-derived stem cells
Choi, Yu Suk, Matsuda, Ken, Dusting, Gregory, Morrison, Wayne and Dilley, Rodney J.. (2010). Engineering cardiac tissue in vivo from human adipose-derived stem cells. Biomaterials. 31(8), pp. 2236 - 2242. https://doi.org/10.1016/j.biomaterials.2009.11.097
Implanted Myoblast Survival Is Dependent on the Degree of Vascularization in a NovelDelayed Implantation/Prevascularization Tissue Engineering Model
Tilkorn, Daniel J., Bedogni, Alberto, Keramidaris, Efthimia, Han, Xiao-Lian, Palmer, Jason, Dingle, Aaron M., Cowling, Belinda Simone, Williams, Michael D., McKay, Sue M., Pepe, Liliana, Deftereos, Anna, Morrison, Wayne, Penington, Tony and Mitchell, Geraldine. (2010). Implanted Myoblast Survival Is Dependent on the Degree of Vascularization in a NovelDelayed Implantation/Prevascularization Tissue Engineering Model. Tissue Engineering Part A. 16(1), pp. 165 - 178. https://doi.org/10.1089/ten.tea.2009.0075
Epoxy-amine synthesised hydrogel scaffolds for soft-tissue engineering
Hamid, Zuratul A. A., Blencowe, Anton, Ozcelik, Berkay, Palmer, Jason, Stevens, Geoffrey W., Abberton, Keren, Morrison, Wayne, Penington, Tony and Qiao, Greg G.. (2010). Epoxy-amine synthesised hydrogel scaffolds for soft-tissue engineering. Biomaterials. 31(25), pp. 6454 - 6467. https://doi.org/10.1016/j.biomaterials.2010.05.008
Differentiation of human adipose-derived stem cells into beating cardiomyocytes
Choi, Yu Suk, Dusting, Gregory, Stubbs, Samantha, Arunothayaraj, Sandeep, Han, Xiao-Lian, Collas, Philippe, Morrison, Wayne and Dilley, Rodney J.. (2010). Differentiation of human adipose-derived stem cells into beating cardiomyocytes. Journal of Cellular and Molecular Medicine. 14(4), pp. 878 - 889. https://doi.org/10.1111/j.1582-4934.2010.01009.x
Zymosan-induced inflammation stimulates neo-adipogenesis
Thomas, Gregory P., Hemmrich, Karsten, Abberton, Keren, McCombe, David B., Penington, Tony, Thompson, Erik and Morrison, Wayne. (2008). Zymosan-induced inflammation stimulates neo-adipogenesis. International Journal of Obesity. 32(2), pp. 239 - 248. https://doi.org/10.1038/sj.ijo.0803702
An endogenously deposited fibrin scaffold determines construct size in the surgicallycreated arteriovenous loop chamber model of tissue engineering
Lokmic, Zerina, Thomas, James L., Morrison, Wayne, Thompson, Erik and Mitchell, Geraldine. (2008). An endogenously deposited fibrin scaffold determines construct size in the surgicallycreated arteriovenous loop chamber model of tissue engineering. Journal of Vascular Surgery. 48(4), pp. 974 - 985. https://doi.org/10.1016/j.jvs.2008.05.021
Neovascularization in an arterio-venous loop-containing tissue engineering chamber: Role of NADPH oxidase
Jiang, Fan, Zhang, G., Hashimoto, Ichiro, Kumar, Beena S., Bortolotto, Susan K., Morrison, Wayne and Dusting, Gregory. (2008). Neovascularization in an arterio-venous loop-containing tissue engineering chamber: Role of NADPH oxidase. Journal of Cellular and Molecular Medicine. 12(5B), pp. 2062 - 2072. https://doi.org/10.1111/j.1582-4934.2008.00199.x
Myogel, a novel, basement membrane-rich, extracellular matrix derived from skeletal muscle, is highly adipogenic in vivo and in vitro
Abberton, Keren, Bortolotto, Susan K., Woods, Alan A., Findlay, Michael W., Morrison, Wayne, Thompson, Erik and Messina, Aurora. (2008). Myogel, a novel, basement membrane-rich, extracellular matrix derived from skeletal muscle, is highly adipogenic in vivo and in vitro. Cells, Tissues, Organs: in vivo, in vitro. 188(4), pp. 347 - 358. https://doi.org/10.1159/000121575
Reconstruction after external hemipelvectomy using tibia-hindfoot rotationplasty with calcaneo-sacral fixation
Kong, George Y. X., Rudiger, Hannes A., Ek, Eugene T. H., Morrison, Wayne and Choong, Peter F. M.. (2008). Reconstruction after external hemipelvectomy using tibia-hindfoot rotationplasty with calcaneo-sacral fixation. International Seminars in Surgical Oncology. 5(Article 1), pp. 1 - 4. https://doi.org/10.1186/1477-7800-5-1
Adipose differentiation of bone marrow-derived mesenchymal stem cells using Pluronic F-127 hydrogel in vitro
Vashi, Aditya V., Keramidaris, Efthimia, Abberton, Keren, Morrison, Wayne, Wilson, Jeremy L., O'Connor, Andrea J., Cooper-White, Justin J. and Thompson, Erik. (2008). Adipose differentiation of bone marrow-derived mesenchymal stem cells using Pluronic F-127 hydrogel in vitro. Biomaterials. 29(5), pp. 573 - 579. https://doi.org/10.1016/j.biomaterials.2007.10.017