Mesenchymal stem cells support hepatocyte function in engineered liver grafts

Organogenesis

Volumn 10, Issue 2, 2014, Pages 268-277

  Kadota, Yoshie ^a   Yagi, Hiroshi ^a   Inomata, Kenta ^a   Matsubara, Kentaro ^a   Hibi, Taizo ^a   Abe, Yuta ^a   Kitago, Minoru ^a   Shinoda, Masahiro ^a   Obara, Hideaki ^a   Itano, Osamu ^a   Kitagawa, Yuko ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Cell transplantation; Organ transplantation; Regenerative medicine; Scaffold matrix; Stem cell; Tissue engineering

Indexed keywords

ALBUMIN; BETA1 INTEGRIN; UREA; VASCULOTROPIN; ANGIOGENIC FACTOR; CELL ADHESION MOLECULE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; ARTIFICIAL LIVER; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL ADHESION; CELL COUNT; CELL ISOLATION; CELL MIGRATION; CELL TRACKING; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; LIVER CELL; LIVER FUNCTION; LIVER GRAFT; LIVER REGENERATION; NICK END LABELING; NONHUMAN; ORGAN PRESERVATION; PARACRINE SIGNALING; PORTAL VEIN BLOOD FLOW; PROTEIN EXPRESSION; RAT; STABLE EXPRESSION; TISSUE ENGINEERING; TISSUE SCAFFOLD; UPREGULATION; ANIMAL; CHEMISTRY; CYTOLOGY; LEWIS RAT; LIVER; LIVER TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; PROCEDURES;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELL ADHESION MOLECULES; CELL COUNT; FEMALE; HEPATOCYTES; LIVER; LIVER TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; RATS, INBRED LEW; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84907509516     PISSN: 15476278     EISSN: 15558592     Source Type: Journal    
DOI: 10.4161/org.27879     Document Type: Article

References (50)

1. Wertheim JA, Petrowsky H, Saab S, Kupiec-Weglinski JW, Busuttil RW. Major challenges limiting liver transplantation in the United States. Am J Transplant 2011; 11:1773-84; PMID:21672146; http://dx.doi.org/10.1111/j.1600-6143.2011.03587.x
2. Kim WR, Stock PG, Smith JM, Heimbach JK, Skeans MA, Edwards EB, Harper AM, Snyder JJ, Israni AK, Kasiske BL. OPTN/SRTR 2011 Annual Data Report: liver. Am J Transplant 2013; 13(Suppl 1):73-102; PMID:23237697; http://dx.doi.org/10.1111/ajt.12021
3. Fox IJ, Chowdhury JR, Kaufman SS, Goertzen TC, Chowdhury NR, Warkentin PI, Dorko K, Sauter BV, Strom SC. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N Engl J Med 1998; 338:1422-6; PMID:9580649; http://dx.doi.org/10.1056/NEJM199805143382004
4. Vacanti JP, Morse MA, Saltzman WM, Domb AJ, Perez-Atayde A, Langer R. Selective cell transplantation using bioabsorbable artificial polymers as matrices. J Pediatr Surg 1988; 23:3-9; PMID:2895175; http://dx.doi.org/10.1016/S0022-3468(88)80529-3
5. Demetriou AA, Whiting JF, Feldman D, Levenson SM, Chowdhury NR, Moscioni AD, Kram M, Chowdhury JR. Replacement of liver function in rats by transplantation of microcarrier-attached hepatocytes. Science 1986; 233:1190-2; PMID:2426782; http://dx.doi.org/10.1126/science.2426782
6. Uygun BE, Soto-Gutierrez A, Yagi H, Izamis ML, Guzzardi MA, Shulman C, Milwid J, Kobayashi N, Tilles A, Berthiaume F, et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med 2010; 16:814-20; PMID:20543851; http://dx.doi.org/10.1038/nm.2170
7. Ott HC, Clippinger B, Conrad C, Schuetz C, Pomerantseva I, Ikonomou L, Kotton D, Vacanti JP. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 2010; 16:927-33; PMID:20628374; http://dx.doi.org/10.1038/nm.2193
8. Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 2008; 14:213-21; PMID:18193059; http://dx.doi.org/10.1038/nm1684
9. Song JJ, Guyette JP, Gilpin SE, Gonzalez G, Vacanti JP, Ott HC. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med 2013; 19:646-51; PMID:23584091; http://dx.doi.org/10.1038/nm.3154
10. Badylak SF, Taylor D, Uygun K. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 2011; 13:27-53; PMID:21417722; http://dx.doi.org/10.1146/annurev-bioeng-071910-124743
11. Earle WR, Schilling EL, Shannon JE Jr. Growth of animal tissue cells on three-dimensional substrates. J Natl Cancer Inst 1951; 12:179-93; PMID:14874128
12. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005; 23:47-55; PMID:15637621; http://dx.doi.org/10.1038/nbt1055
13. Gilbert TW, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomaterials 2006; 27:3675-83; PMID:16519932
14. Soto-Gutierrez A, Zhang L, Medberry C, Fukumitsu K, Faulk D, Jiang H, Reing J, Gramignoli R, Komori J, Ross M, et al. A whole-organ regenerative medicine approach for liver replacement. Tissue Eng Part C Methods 2011; 17:677-86; PMID:21375407; http://dx.doi.org/10.1089/ten.tec.2010.0698
15. Zhou P, Lessa N, Estrada DC, Severson EB, Lingala S, Zern MA, Nolta JA, Wu J. Decellularized liver matrix as a carrier for the transplantation of human fetal and primary hepatocytes in mice. Liver Transpl 2011; 17:418-27; PMID:21445925; http://dx.doi.org/10.1002/lt.22270
16. Baptista PM, Siddiqui MM, Lozier G, Rodriguez SR, Atala A, Soker S. The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatology 2011; 53:604-17; PMID:21274881; http://dx.doi.org/10.1002/hep.24067
17. Bao J, Shi Y, Sun H, Yin X, Yang R, Li L, Chen X, Bu H. Construction of a portal implantable functional tissue-engineered liver using perfusion-decellularized matrix and hepatocytes in rats. Cell Transplant 2011; 20:753-66; PMID:21054928; http://dx.doi.rg/10.3727/096368910X536572
18. Barakat O, Abbasi S, Rodriguez G, Rios J, Wood RP, Ozaki C, Holley LS, Gauthier PK. Use of decellularized porcine liver for engineering humanized liver organ. J Surg Res 2012; 173:e11-25; PMID:22099595; http://dx.doi.org/10.1016/j. jss.2011.09.033
19. Yagi H, Fukumitsu K, Fukuda K, Kitago M, Shinoda M, Obara H, Itano O, Kawachi S, Tanabe M, Coudriet GM, et al. Human-scale wholeorgan bioengineering for liver transplantation: A regenerative medicine approach. Cell Transplant 2013; 22:231-42; PMID:22943797; http://dx.doi.org/10.3727/096368912X654939
20. Soto-Gutiérrez A, Navarro-Alvarez N, Zhao D, Rivas-Carrillo JD, Lebkowski J, Tanaka N, Fox IJ, Kobayashi N. Differentiation of mouse embryonic stem cells to hepatocyte-like cells by co-culture with human liver nonparenchymal cell lines. Nat Protoc 2007; 2:347-56; PMID:17406596; http://dx.doi.org/10.1038/nprot.2007.18
21. McClelland R, Wauthier E, Uronis J, Reid L. Gradients in the liver's extracellular matrix chemistry from periportal to pericentral zones: influence on human hepatic progenitors. Tissue Eng Part A 2008; 14:59-70; PMID:18333805; http://dx.doi.org/10.1089/ten.a.2007.0058
22. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418:41-9; PMID:12077603; http://dx.doi.org/10.1038/nature00870
23. Yagi H, Soto-Gutierrez A, Navarro-Alvarez N, Nahmias Y, Goldwasser Y, Kitagawa Y, Tilles AW, Tompkins RG, Parekkadan B, Yarmush ML. Reactive bone marrow stromal cells attenuate systemic inflammation via sTNFR1. Mol Ther 2010; 18:1857-64; PMID:20664529; http://dx.doi.org/10.1038/mt.2010.155
24. Yagi H, Soto-Gutierrez A, Parekkadan B, Kitagawa Y, Tompkins RG, Kobayashi N, Yarmush ML. Mesenchymal stem cells: Mechanisms of immunomodulation and homing. Cell Transplant 2010; 19:667-79; PMID:20525442; http://dx.doi.org/10.3727/096368910X508762
25. Yagi H, Parekkadan B, Suganuma K, Soto-Gutierrez A, Tompkins RG, Tilles AW, Yarmush ML. Longterm superior performance of a stem cell/hepatocyte device for the treatment of acute liver failure. Tissue Eng Part A 2009; 15:3377-88; PMID:19397469; http://dx.doi.org/10.1089/ten.tea.2008.0681
26. Takebe T, Sekine K, Enomura M, Koike H, Kimura M, Ogaeri T, Zhang RR, Ueno Y, Zheng YW, Koike N, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 2013; 499:481-4; PMID:23823721; http://dx.doi.org/10.1038/nature12271
27. Xu H, Shi BM, Lu XF, Liang F, Jin X, Wu TH, Xu J. Vascular endothelial growth factor attenuates hepatic sinusoidal capillarization in thioacetamide-induced cirrhotic rats. World J Gastroenterol 2008; 14:2349-57; PMID:18416461; http://dx.doi.org/10.3748/wjg.14.2349
28. Wang L, Wang X, Wang L, Chiu JD, van de Ven G, Gaarde WA, Deleve LD. Hepatic vascular endothelial growth factor regulates recruitment of rat liver sinusoidal endothelial cell progenitor cells. Gastroenterology 2012; 143:1555-63, e2; PMID:22902870; http://dx.doi.org/10.1053/j.gastro.2012.08.008
29. Sugiyama Y, Takabe Y, Nakakura T, Tanaka S, Koike T, Shiojiri N. Sinusoid development and morphogenesis may be stimulated by VEGF-Flk-1 signaling during fetal mouse liver development. Dev Dyn 2010; 239:386-97; PMID:19918884; http://dx.doi.org/10.1002/dvdy.22162
30. Matsumoto K, Yoshitomi H, Rossant J, Zaret KS. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 2001; 294:559-63; PMID:11577199; http://dx.doi.org/10.1126/science.1063889
31. Carvalho S, Cortez E, Stumbo AC, Thole A, Caetano C, Marques R, Pelajo-Machado M, Porto LC, Carvalho L. Laminin expression during bone marrow mononuclear cell transplantation in hepatectomized rats. Cell Biol Int 2008; 32:1014-8; PMID:18485749; http://dx.doi.org/10.1016/j.cellbi.2008.04.003
32. Alison MR, Golding M, Sarraf CE, Edwards RJ, Lalani EN. Liver damage in the rat induces hepatocyte stem cells from biliary epithelial cells. Gastroenterology 1996; 110:1182-90; PMID:8613008; http://dx.doi.org/10.1053/gast.1996.v110.pm8613008
33. Oh SH, Witek RP, Bae SH, Zheng D, Jung Y, Piscaglia AC, Petersen BE. Bone marrow-derived hepatic oval cells differentiate into hepatocytes in 2-acetylaminofluorene/partial hepatectomy-induced liver regeneration. Gastroenterology 2007; 132:1077-87; PMID:17383429; http://dx.doi.org/10.1053/j. gastro.2007.01.001
34. Soto-Gutierrez A, Wertheim JA, Ott HC, Gilbert TW. Perspectives on whole-organ assembly: moving toward transplantation on demand. J Clin Invest 2012; 122:3817-23; PMID:23114604; http://dx.doi.org/10.1172/JCI61974
35. Uygun BE, Yarmush ML, Uygun K. Application of whole-organ tissue engineering in hepatology. Nat Rev Gastroenterol Hepatol 2012; 9:738-44; http://dx.doi.org/10.1038/nrgastro.2012.140
36. Suzuki A, Zheng YW, Kaneko S, Onodera M, Fukao K, Nakauchi H, Taniguchi H. Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver. J Cell Biol 2002; 156:173-84; PMID:11781341; http://dx.doi.org/10.1083/jcb.200108066
37. Oertel M, Menthena A, Chen YQ, Teisner B, Jensen CH, Shafritz DA. Purification of fetal liver stem/progenitor cells containing all the repopulation potential for normal adult rat liver. Gastroenterology 2008; 134:823-32; PMID:18262526; http://dx.doi.org/10.1053/j.gastro.2008.01.007
38. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002; 99:3838-43; PMID:11986244; http://dx.doi.org/10.1182/blood.V99.10.3838
39. Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 2006; 24:74-85; PMID:16099998; http://dx.doi.org/10.1634/stemcells.2004-0359
40. Wang Y, Yao HL, Cui CB, Wauthier E, Barbier C, Costello MJ, Moss N, Yamauchi M, Sricholpech M, Gerber D, et al. Paracrine signals from mesenchymal cell populations govern the expansion and differentiation of human hepatic stem cells to adult liver fates. Hepatology 2010; 52:1443-54; PMID:20721882; http://dx.doi.org/10.1002/hep.23829
41. Beckermann BM, Kallifatidis G, Groth A, Frommhold D, Apel A, Mattern J, Salnikov AV, Moldenhauer G, Wagner W, Diehlmann A, et al. VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer 2008; 99:622-31; PMID:18665180; http://dx.doi.org/10.1038/sj.bjc.6604508
42. Stolz DB, Ross MA, Ikeda A, Tomiyama K, Kaizu T, Geller DA, Murase N. Sinusoidal endothelial cell repopulation following ischemia/reperfusion injury in rat liver transplantation. Hepatology 2007; 46:1464-75; PMID:17929236; http://dx.doi.org/10.1002/hep.21887
43. Fässler R, Meyer M. Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 1995; 9:1896-908; PMID:7544313; http://dx.doi.org/10.1101/gad.9.15.1896
44. Kim SH, Turnbull J, Guimond S. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J Endocrinol 2011; 209:139-51; PMID:21307119; http://dx.doi.org/10.1530/JOE-10-0377
45. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126:677-89; PMID:16923388; http://dx.doi.org/10.1016/j.cell.2006.06.044
46. Discher DE, Mooney DJ, Zandstra PW. Growth factors, matrices, and forces combine and control stem cells. Science 2009; 324:1673-7; PMID:19556500; http://dx.doi.org/10.1126/science.1171643
47. Kallis YN, Robson AJ, Fallowfield JA, Thomas HC, Alison MR, Wright NA, Goldin RD, Iredale JP, Forbes SJ. Remodelling of extracellular matrix is a requirement for the hepatic progenitor cell response. Gut 2011; 60:525-33; PMID:21106552; http://dx.doi.org/10.1136/gut.2010.224436
48. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005; 433:760-4; PMID:15716955; http://dx.doi.org/10.1038/nature03260
49. Moolten FL, Bucher NL. Regeneration of rat liver: transfer of humoral agent by cross circulation. Science 1967; 158:272-4; PMID:6053886; http://dx.doi.org/10.1126/science.158.3798.272
50. Kato Y, Shimazu M, Wakabayashi G, Tanabe M, Morikawa Y, Hoshino K, Harada H, Kadomura T, Obara H, Urakami H, et al. Significance of portal venous flow in graft regeneration after living related liver transplantation. Transplant Proc 2001; 33:1484-5; PMID:11267384; http://dx.doi.org/10.1016/S0041-1345(00)02562-8