Sodium butyrate-treated embryonic stem cells yield hepatocyte-like cells expressing a glycolytic phenotype

Biotechnology and Bioengineering

Volumn 94, Issue 6, 2006, Pages 1053-1063

  Sharma, N S ^a   Shikhanovich, R ^b   Schloss, R ^b   Yarmush, M L ^a,b  

^a The State University of New Jersey   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Energy metabolism; Hepatocyte like cells; Sodium butyrate

Indexed keywords

ASSAYS; CELL CULTURE; GLYCOLS; METABOLISM; MONOLAYERS; SODIUM COMPOUNDS;

ENERGY METABOLISM; HEPATOCYTE-LIKE CELLS; SODIUM BUTYRATE;

CELLS;

ALBUMIN; BUTYRIC ACID; CYTOKERATIN 18; GLYCOGEN; UREA;

AEROBIC CAPACITY; ANIMAL CELL; ARTICLE; BIOENERGY; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CELL TYPE; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENERGY METABOLISM; ENERGY TRANSFER; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLYCOLYSIS; HEART MUSCLE CELL; LIVER CELL; MITOCHONDRION; MOUSE; NERVE CELL; NONHUMAN; OXIDATION; PHENOTYPE; PHOSPHORYLATION;

BUTYRATES; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; GLUCOSE; GLYCOGEN; GLYCOLYSIS; HEPATOCYTES; METABOLIC CLEARANCE RATE; MICE; MITOCHONDRIA; STEM CELLS; TISSUE ENGINEERING;

MURINAE;

EID: 33747111033     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.20936     Document Type: Article

References (58)

1. Abe K, Niwa H, Iwase K, Takiguchi M, Mori M, Abe SI, Yamamura KI. 1996. Endoderm-specific gene expression in embryonic stem cells differentiated to embryoid bodies. Exp Cell Res 229(1):27-34.
2. Allen RG, Balin AK. 1989. Oxidative influence on development and differentiation: An overview of a free radical theory of development. Free Radic Biol Med 6(6):631-661.
3. Allen RG, Venkatraj VS. 1992. Oxidants and antioxidants in development and differentiation. J Nutr 122(Suppl 3):631-635.
4. Arias IM, Boyer JL, Fausto N, Jakoby WB, Schacter D, Shafritz DA. 1994. The liver: Biology and pathobiology. New York: Raven. 834.
5. Asahina K, Fujimori H, Shimizu-Saito K, Kumashiro Y, Okamura K, Tanaka Y, Teramoto K, Arii S, Teraoka H. 2004. Expression of the liver-specific gene Cyp7a1 reveals hepatic differentiation in embryoid bodies derived from mouse embryonic stem cells. Genes Cells 9(12):1297-1308.
6. Berthiaume F, MacDonald AD, Kang YH, Yarmush ML. 2003. Control analysis of mitochondrial metabolism in intact hepatocytes: Effect of interleukin-1beta and interleukin-6. Metab Eng 5(2):108-123.
7. Blouin MJ, Lamy I, Loranger A, Noel M, Corlu A, Guguen-Guillouzo C, Marceau N. 1995. Specialization switch in differentiating embryonic rat liver progenitor cells in response to sodium butyrate. Exp Cell Res 217(1):22-30.
8. Burch HB, Lowry OH, Kuhlman AM, Skerjance J, Diamant EJ, Lowry SR, Von Dippe P. 1963. Changes in patterns of enzymes of carbohydrate metabolism in the developing rat liver. J Biol Chem 238:2267-2273.
9. Cai YF, Zhen ZJ, Min J, Fang TL, Chu ZH, Chen JS. 2004. Selection, proliferation and differentiation of bone marrow-derived liver stem cells with a culture system containing cholestatic serum in vitro. World J Gastroenterol 10(22):3308-3312.
10. Chan C, Berthiaume F, Lee K, Yarmush ML. 2003. Metabolic flux analysis of cultured hepatocytes exposed to plasma. Biotechnol Bioeng 81(1): 33-49.
11. Chan C, Berthiaume F, Nath BD, Tilles AW, Toner M, Yarmush ML. 2004. Hepatic tissue engineering for adjunct and temporary liver support: Critical technologies. Liver Transpl 10(11):1331-1342.
12. Chinzei R, Tanaka Y, Shimizu-Saito K, Hara Y, Kakinuma S, Watanabe M, Teramoto K, Arii S, Takase K, Sato C, Terada N, Teraoka H. 2002. Embryoid-body cells derived from a mouse embryonic stem cell line show differentiation into functional hepatocytes. Hepatology 36(1): 22-29.
13. Choi D, Oh HJ, Chang UJ, Koo SK, Jiang JX, Hwang SY, Lee JD, Yeoh GC, Shin HS, Lee JS, Oh B. 2002. In vivo differentiation of mouse embryonic stem cells into hepatocytes. Cell Transplant 11(4):359-368.
14. Cuezva JM, Ostronoff LK, Ricart J, Lopez de Heredia M, Di Liegro CM, Izquierdo JM. 1997. Mitochondrial biogenesis in the liver during development and oncogenesis. J Bioenerg Biomembr 29(4):365-377.
15. David H. 1979. Quantitative and qualitative changes in the mitochondria in hepatocytes during postnatal development of male rats. Exp Pathol (Jena) 17(7-8):359-373.
16. Devreker F, Englert Y. 2000. In vitro development and metabolism of the human embryo up to the blastocyst stage. Eur J Obstet Gynecol Reprod Biol 92(1):51-56.
17. Dittmann L, Hertz L, Schousboe A, Fosmark H, Sensenbrenner M, Mandel P. 1973. Energy metabolism of nerve cells during differentiation. O2 uptake, lactate production and ATP content of chick embryo brain cells before and after cultivation in the Rose chamber. Exp Cell Res 80(2): 425-431.
18. Hamazaki T, Iiboshi Y, Oka M, Papst PJ, Meacham AM, Zon LI, Terada N. 2001. Hepatic maturation in differentiating embryonic stem cells in vitro. FEBS Lett 497(1): 15-19.
19. Harvey AJ, Kind KL, Thompson JG. 2002. REDOX regulation of early embryo development. Reproduction 123(4):479-486.
20. Hayashi K, Ochiai T, Ishinoda Y, Okamoto T, Maruyama T, Tsuda K, Tsubouchi H. 1997. Relationship between cellular ATP content and cellular functions of primary cultured rat hepatocytes in hypoxia. J Gastroenterol Hepatol 12(3):249-256.
21. Hewitson LC, Leese HJ. 1993. Energy metabolism of the trophectoderm and inner cell mass of the mouse blastocyst. J Exp Zool 267(3):337-343.
22. Houghton FD, Thompson JG, Kennedy CJ, Leese HJ. 1996. Oxygen consumption and energy metabolism of the early mouse embryo. Mol Reprod Dev 44(4):476-485.
23. Imamura T, Cui L, Teng R, Johkura K, Okouchi Y, Asanuma K, Ogiwara N, Sasaki K. 2004. Embryonic stem cell-derived embryoid bodies in three-dimensional culture system form hepatocyte-like cells in vitro and in vivo. Tissue Eng 10(11-12):1716-1724.
24. Ishizaka S, Shiroi A, Kanda S, Yoshikawa M, Tsujinoue H, Kuriyama S, Hasuma T, Nakatani K, Takahashi K. 2002. Development of hepatocytes from ES cells after transfection with the HNF-3beta gene. Faseb J 16(11):1444-1446.
25. Iwai M, Tanaka S, Mori T, Harada Y, Muramatsu A, Morikawa T, Kashima K, Fushiki S. 2002. Investigation of parenchymal cell differentiation in organotypic slice culture of mouse fetal liver under administration of sodium butyrate. Cell Biol Toxicol 18(3):147-156.
26. Kim M, Cooper DD, Hayes SF, Spangrude GJ. 1998. Rhodamine-123 staining in hematopoietic stem cells of young mice indicates mitochondrial activation rather than dye efflux. Blood 91(11):4106-4117.
27. Komarova SV, Ataullakhanov FI, Globus RK. 2000. Bioenergetics and mitochondrial transmembrane potential during differentiation of cultured osteoblasts. Am J Physiol Cell Physiol 279(4):C1220-C1229.
28. Lee HC, Yin PH, Lu CY, Chi CW, Wei YH. 2000. Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J 348 Pt 2, 425-432.
29. Lovtrup-Rein H, Nelson L. 1982. Changes in energy metabolism during the early development of Xenopus laevis. Exp Cell Biol 50(3):162-168.
30. Marinos E, Billett FS. 1981. Mitochondrial number, cytochrome oxidase and succinic dehydrogenase activity in Xenopus laevis oocytes. J Embryol Exp Morphol 62:395-409.
31. Moll R, Franke WW, Schiller DL, Geiger B, Krepier R. 1982. The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells. Cell 31(1):11-24.
32. Newmark HL, Young CW. 1995. Butyrate and phenylacetate as differentiating agents: Practical problems and opportunities. J Cell Biochem Suppl 22:247-253.
33. Novik EN, Maguire TJ, Schloss R, Yarmush ML. 2006. Generating a tissue culture platform for the differentiation of ES cells into functional hepatocytes. Tissue Eng. (In press).
34. Odorico JS, Kaufman DS, Thomson JA. 2001. Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19(3):193-204.
35. Okuda KI. 1994. Liver mitochondrial P450 involved in cholesterol catabolism and vitamin D activation. J Lipid Res 35(3):361-372.
36. Oliver IT, Martin RL, Fisher CJ, Yeoh GC. 1983. Enzymic differentiation in cultured foetal hepatocytes of the rat. Induction of serine dehydratase activity by dexamethasone and dibutyryl cyclic AMP. Differentiation 24(3):234-238.
37. Papaconstantinou P. 1967. The biochemistry of animal development, biochemical control mechanisms and adaptations in development. Vol II, Academic press, Chpt 2, Metabolic Control of Growth and Differentiation in vertebrate embryos. 59-84.
38. Petit JM, Maftah A, Ratinaud MH, Julien R. 1992. 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur J Biochem 209(1):267-273.
39. Petit JM, Huet O, Gallet PF, Maftah A, Ratinaud MH, Julien R. 1994. Direct analysis and significance of cardiolipin transverse distribution in mitochondrial inner membranes. Eur J Biochem 220(3):871-879.
40. Phillips JW, Jones ME, Berry MN. 2002. Implications of the simultaneous occurrence of hepatic glycolysis from glucose and gluconeogenesis from glycerol. Eur J Biochem 269(3):792-797.
41. Pieri C, Nagy Z, Mazzufferi G, Giuli C. 1975. The aging of rat liver as revealed by electron microscopic morphometry-I. Basic parameters. Exp Gerontol 10(5):291-304.
42. Pollak JK. 1975. The maturation of the inner membrane of foetal rat liver mitochondria. Biochem J 150(3):477-488.
43. Pollak JK, Duck-Chong CG. 1973. Changes in rat liver mitochondria and endoplasmic reticulum during development and differentiation. Enzyme 15(1):139-160.
44. Rambhatla L, Chiu CP, Kundu P, Peng Y, Carpenter MK. 2003. Generation of hepatocyte-like cells from human embryonic stem cells. Cell Transplant 12(1):1-11.
45. Richard D, Hollender P, Chenais B. 2002. Butyric acid increases invasiveness of HL-60 leukemia cells: Role of reactive oxygen species. FEBS Lett 518(1-3):159-163.
46. Rohr HP, Wacker M, Pein AV. 1976. Ethidium bromide and hepatic mitochondrial structure in mice. A morphometric analysis. Pathol Eur 11(2):129-135.
47. Rosato RR, Wang Z, Gopalkrishnan RV, Fisher PB, Grant S. 2001. Evidence of a functional role for the cyclin-dependent kinase-inhibitor p21WAF1/CIP1/MDA6 in promoting differentiation and preventing mitochondrial dysfunction and apoptosis induced by sodium butyrate in human myelomonocytic leukemia cells (U937). Int J Oncol 19(1):181-191.
48. Schuldiner M, Yanuka O, Itskovitz-Eldor J, Melton DA, Benvenisty N. 2000. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 97(21): 11307-11312.
49. Sharma NS, Ierapetritou MG, Yarmush ML. 2005. Novel quantitative tools for engineering analysis of hepatocyte cultures in bioartificial liver systems. Biotechnol Bioeng 92(3):321-335.
50. Shelly LL, Tynan W, Schmid W, Schutz G, Yeoh GC. 1989. Hepatocyte differentiation in vitro: Initiation of tyrosine aminotransferase expression in cultured fetal rat hepatocytes. J Cell Biol 109(6 Pt 2):3403-3410.
51. Shishido S, Koga H, Harada M, Kumemura H, Hanada S, Taniguchi E, Kumashiro R, Ohira H, Sato Y, Namba M, Ueno T, Sata M. 2003. Hydrogen peroxide overproduction in megamitochondria of troglitazone-treated human hepatocytes. Hepatology 37(1):136-147.
52. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145-1147.
53. Vergonet G, Hommes FA, Molenaar I. 1970. A morphometric and biochemical study of fetal and adult rat liver cells, with special reference to energy metabolism. Biol Neonate 16(5):297-305.
54. von Wangenheim KH, Peterson HP. 1998. Control of cell proliferation by progress in differentiation: Clues to mechanisms of aging, cancer causation and therapy. J Theor Biol 193(4):663-678.
55. Waki A, Yano R, Yoshimoto M, Sadato N, Yonekura Y, Fujibayashi Y. 2001. Dynamic changes in glucose metabolism accompanying the expression of the neural phenotype after differentiation in PC12 cells. Brain Res 894(1):88-94.
56. Watt AJ, Jones EA, Ure JM, Peddie D, Wilson DI, Forrester LM. 2001. A gene trap integration provides an early in situ marker for hepatic specification of the foregut endoderm. Mech Dev 100(2):205-215.
57. Yamamoto Y, Teratani T, Yamamoto H, Quinn G, Murata S, Ikeda R, Kinoshita K, Matsubara K, Kato T, Ochiya T. 2005. Recapitulation of in vivo gene expression during hepatic differentiation from murine embryonic stem cells. Hepatology 42(3):558-567.
58. Yarmush ML, Toner M, Dunn JC, Rotem A, Hubel A, Tompkins RG. 1992. Hepatic tissue engineering. Development of critical technologies. Ann N Y Acad Sci 665:238-252.