Top

Published in:

01-12-2017 | Original Article

Hepatocytic differentiation of iPS cells on decellularized liver tissue

Authors: Mitsuhi Hirata, Tetsuji Yamaoka

Published in: Journal of Artificial Organs | Issue 4/2017

Abstract

Decellularized tissues (DETs) have been attracting great attention as scaffolds for tissue-engineering approaches. Recently, some studies have reported that decellularized liver tissues (DLT) can provide an excellent environment for the hepatocytic differentiation of hepatic stem/progenitor cells that were already committed to the hepatocyte lineage. However, the effects of DLT on the hepatocytic differentiation of induced pluripotent stem cells (iPSs) have not yet been established. Here we studied the hepatocytic differentiation of iPSs on DLT and decellularized heart tissues (DHT) in order to determine the tissue-specific effects of DETs on iPSs differentiation. Our results showed that DLTs led to higher gene expression levels of forkhead box A2 (a marker of endoderm) and CCAAT/enhancer binding protein-α (master transcription factor to hepatocyte differentiation), alpha-fetoprotein (a marker of fetal hepatocyte,), and albumin (a marker of fetal and mature hepatocyte) of iPSs than on DHTs. Furthermore, gene expression levels of tyrosine aminotransferase (a marker of mature hepatocyte) were higher on DLT than that on DHT, and immunocytochemical analysis and ELISA assay showed that albumin secretion level of iPSs on DLT was higher than that on DHT. Our study demonstrated that the use of DLTs led to mature hepatocytic differentiation levels of iPSs compared to DHTs, which provides a better niche for iPSs cell engineering and enables the preparation of useful mature cells for regenerative therapy.

Available only for authorised users

Fox IJ, Roy-Chowdhury J. Hepatocyte transplantation. J Hepatol. 2004;40:878–86.CrossRefPubMed

Fox IJ, Chowdhury JR, Kaufman SS, Goertzen TC, Chowdhury NR, Warkentin PI, et al. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N Engl J Med. 1998;338:1422–6.CrossRefPubMed

Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, et al. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14:213–21.CrossRefPubMed

Gilbert TW, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomaterials. 2006;27:3675–83.PubMed

Vesely I. Heart valve tissue engineering. Circ Res. 2005;97:743–55.CrossRefPubMed

Crapo PM, Medberry CJ, Reing JE, Tottey S, van der Merwe Y, Jones KE, et al. Biologic scaffolds composed of central nervous system extracellular matrix. Biomaterials. 2012;33:3539–47.CrossRefPubMedPubMedCentral

Neubauer D, Graham JB, Muir D. Chondroitinase treatment increases the effective length of acellular nerve grafts. Exp Neurol. 2007;207:163–70.CrossRefPubMedPubMedCentral

Hashimoto Y, Funamoto S, Sasaki S, Honda T, Hattori S, Nam K, et al. Preparation and characterization of decellularized cornea using high-hydrostatic pressurization for corneal tissue engineering. Biomaterials. 2010;31:3941–8.CrossRefPubMed

Fu Y, Fan X, Chen P, Shao C, Lu W. Reconstruction of a tissue-engineered cornea with porcine corneal acellular matrix as the scaffold. Cells, Tissues, Organs. 2010;191:193–202.CrossRefPubMed

10.

Eberli D, Rodriguez S, Atala A, Yoo JJ. In vivo evaluation of acellular human dermis for abdominal wall repair. J Biomed Mater Res, Part A. 2010;93:1527–38.

11.

Ng SL, Narayanan K, Gao S, Wan AC. Lineage restricted progenitors for the repopulation of decellularized heart. Biomaterials. 2011;32:7571–80.CrossRefPubMed

12.

Lu TY, Lin B, Kim J, Sullivan M, Tobita K, Salama G, et al. Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat Commun. 2013;4:2307.PubMed

13.

Higuchi S, Lin Q, Wang J, Lim TK, Joshi SB, Anand GS, et al. Heart extracellular matrix supports cardiomyocyte differentiation of mouse embryonic stem cells. J Biosci Bioeng. 2013;115:320–5.CrossRefPubMed

14.

Uygun BE, Soto-Gutierrez A, Yagi H, Izamis ML, Guzzardi MA, Shulman C, et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med. 2010;16:814–20.CrossRefPubMedPubMedCentral

15.

Soto-Gutierrez A, Zhang L, Medberry C, Fukumitsu K, Faulk D, Jiang H, et al. A whole-organ regenerative medicine approach for liver replacement. Tissue Eng Part C, Methods. 2011;17:677–86.CrossRef

16.

Wang Y, Cui CB, Yamauchi M, Miguez P, Roach M, Malavarca R, et al. Lineage restriction of human hepatic stem cells to mature fates is made efficient by tissue-specific biomatrix scaffolds. Hepatology (Baltimore, MD). 2011;53:293–305.CrossRef

17.

Barakat O, Abbasi S, Rodriguez G, Rios J, Wood RP, Ozaki C, et al. Use of decellularized porcine liver for engineering humanized liver organ. J Surg Res. 2012;173:e11–25.CrossRefPubMed

18.

Wang X, Cui J, Zhang BQ, Zhang H, Bi Y, Kang Q, et al. Decellularized liver scaffolds effectively support the proliferation and differentiation of mouse fetal hepatic progenitors. J Biomed Mater Res, Part A. 2014;102:1017–25.CrossRef

19.

Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol. 2008;26:101–6.CrossRefPubMed

20.

Zhang Q, Yang Y, Zhang J, Wang GY, Liu W, Qiu DB, et al. Efficient derivation of functional hepatocytes from mouse induced pluripotent stem cells by a combination of cytokines and sodium butyrate. Chin Med J. 2011;124:3786–93.PubMed

21.

Shiojiri N. Enzymo- and immunocytochemical analyses of the differentiation of liver cells in the prenatal mouse. J Embryol Exp Morphol. 1981;62:139–52.PubMed

22.

Jones EA, Clement-Jones M, James OF, Wilson DI. Differences between human and mouse alpha-fetoprotein expression during early development. J Anat. 2001;198:555–9.CrossRefPubMedPubMedCentral

23.

Sellem CH, Frain M, Erdos T, Sala-Trepat JM. Differential expression of albumin and alpha-fetoprotein genes in fetal tissues of mouse and rat. Dev Biol. 1984;102:51–60.CrossRefPubMed

24.

Shiojiri N, Takeshita K, Yamasaki H, Iwata T. Suppression of C/EBP alpha expression in biliary cell differentiation from hepatoblasts during mouse liver development. J Hepatol. 2004;41:790–8.CrossRefPubMed

25.

Greengard O. Enzymic differentiation in mammalian liver injection of fetal rats with hormones causes the premature formation of liver enzymes. Science (New York, NY). 1969;163:891–5.CrossRef

26.

Shelly LL, Tynan W, Schmid W, Schutz G, Yeoh GC. Hepatocyte differentiation in vitro: initiation of tyrosine aminotransferase expression in cultured fetal rat hepatocytes. J Cell Biol. 1989;109:3403–10.CrossRefPubMed

27.

DeQuach JA, Yuan SH, Goldstein LS, Christman KL. Decellularized porcine brain matrix for cell culture and tissue engineering scaffolds. Tissue Eng Part A. 2011;17:2583–92.CrossRefPubMedPubMedCentral

28.

Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677–89.CrossRefPubMed

29.

Shamis Y, Hasson E, Soroker A, Bassat E, Shimoni Y, Ziv T, et al. Organ-specific scaffolds for in vitro expansion, differentiation, and organization of primary lung cells. Tissue Eng Part C, Methods. 2011;17:861–70.CrossRef

30.

Han S, Bourdon A, Hamou W, Dziedzic N, Goldman O, Gouon-Evans V. Generation of functional hepatic cells from pluripotent stem cells. J Stem Cell Res Ther. 2012;Suppl 10:1–7.

31.

Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, Cogan TA, et al. Clinical transplantation of a tissue-engineered airway. Lancet (London, England). 2008;372:2023–30.CrossRef

32.

Bao J, Shi Y, Sun H, Yin X, Yang R, Li L, et al. Construction of a portal implantable functional tissue-engineered liver using perfusion-decellularized matrix and hepatocytes in rats. Cell Transplant. 2011;20:753–66.CrossRefPubMed

33.

Gonfiotti A, Jaus MO, Barale D, Baiguera S, Comin C, Lavorini F, et al. The first tissue-engineered airway transplantation: 5-year follow-up results. Lancet (London, England). 2014;383:238–44.CrossRef

34.

Mahara A, Somekawa S, Kobayashi N, Hirano Y, Kimura Y, Fujisato T, et al. Tissue-engineered acellular small diameter long-bypass grafts with neointima-inducing activity. Biomaterials. 2015;58:54–62.CrossRefPubMed

35.

Hashimoto Y, Funamoto S, Kimura T, Nam K, Fujisato T, Kishida A. The effect of decellularized bone/bone marrow produced by high-hydrostatic pressurization on the osteogenic differentiation of mesenchymal stem cells. Biomaterials. 2011;32:7060–7.CrossRefPubMed

36.

Liem PH, Morimoto N, Mahara A, Jinno C, Shima K, Ogino S, et al. Preparation of Inactivated Human Skin Using High Hydrostatic Pressurization for Full-Thickness Skin Reconstruction. PLoS ONE. 2015;10:e0133979.CrossRefPubMedPubMedCentral

Title: Hepatocytic differentiation of iPS cells on decellularized liver tissue
Authors: Mitsuhi Hirata
Tetsuji Yamaoka
Publication date: 01-12-2017
Publisher: Springer Japan
Published in: Journal of Artificial Organs / Issue 4/2017
Print ISSN: 1434-7229
Electronic ISSN: 1619-0904
DOI: https://doi.org/10.1007/s10047-017-0977-2

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Hepatocytic differentiation of iPS cells on decellularized liver tissue

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2017

Long-term clinical results of acute myocardial infarction at the left main trunk requiring percutaneous cardiopulmonary support

Differences in CVVH vs. CVVHDF in the management of sepsis-induced acute kidney injury in critically ill patients

Veno–veno–arterial extracorporeal membrane oxygenation for acute respiratory distress syndrome with septic-induced cardiomyopathy due to severe pulmonary tuberculosis

Successful management of prolonged venovenous extracorporeal membrane oxygenation in an octogenarian

Readmissions after continuous flow left ventricular assist device implantation

Erratum to: Development of in vivo tissue-engineered microvascular grafts with an ultra small diameter of 0.6 mm (MicroBiotubes): acute phase evaluation by optical coherence tomography and magnetic resonance angiography