Enhanced antioxidant capacity of dental pulp-derived iPSC-differentiated hepatocytes and liver regeneration by injectable HGF-releasing hydrogel in fulminant hepatic failure

Cell Transplantation

Volumn 24, Issue 3, 2015, Pages 541-559

  Chiang, Chih Hung ^a,b   Wu, Wai Wah ^a,c   Li, Hsin Yang ^a,b   Chien, Yueh ^a,b   Sun, Cho Chin ^b   Peng, Chi Hsien ^a,d   Lin, Alex Tong Long ^b   Huang, Chi Shuan ^a,c   Lai, Ying Hsiu ^b   Chiou, Shih Hwa ^a,b   Hung, Shuen Iu ^a   Chang, Yuh Lih ^a,b   Lan, Yuan Tzu ^a,b   Liu, Dean Mo ^e   Chien, Chian Shiu ^a,b   Huo, Teh Ia ^a,b   Lee, Shou Dong ^c   Wang, Chien Ying ^a,b,f  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c CHENG HSIN GENERAL HOSPITAL   (Taiwan)

^d SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^e NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

^f TAJEN UNIVERSITY   (Taiwan)

Author keywords

Acute hepatic failure (AHF); Hepatocyte growth factor (HGF); Hydrogel; Induced pluripotent stem cells (iPSCs)

Indexed keywords

CARBOXYMETHYL HEXANOYL CHITOSAN; CHITOSAN DERIVATIVE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GROWTH DIFFERENTIATION FACTOR 3; KRUPPEL LIKE FACTOR 4; MALONALDEHYDE; MYC PROTEIN; NITRATE; NITRITE; OCTAMER TRANSCRIPTION FACTOR 4; REACTIVE OXYGEN METABOLITE; REX PROTEIN; SCATTER FACTOR; THIOACETAMIDE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; ALANINE AMINOTRANSFERASE; ANTIOXIDANT; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; CARBOXYMETHYL-HEXANOYL CHITOSAN; CHITOSAN; HYDROGEL;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL LINEAGE; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENGRAFTMENT; FIBROBLAST; FULMINANT HEPATIC FAILURE; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; INTRAHEPATIC DRUG ADMINISTRATION; LIVER CELL; LIVER FUNCTION; LIVER NECROSIS; LIVER PROTECTION; LIVER REGENERATION; MALE; MIDDLE AGED; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SUSTAINED DRUG RELEASE; TOOTH PULP; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMICALLY INDUCED; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FEMALE; INSTITUTE FOR CANCER RESEARCH MOUSE; LIVER; LIVER FAILURE, ACUTE; METABOLISM; NUDE MOUSE; PATHOLOGY; TRANSPLANTATION;

ALANINE TRANSAMINASE; ANIMALS; ANTIOXIDANTS; ASPARTATE AMINOTRANSFERASES; BILIRUBIN; CELL DIFFERENTIATION; CELLS, CULTURED; CELLULAR REPROGRAMMING; CHITOSAN; DENTAL PULP; FEMALE; HEPATOCYTE GROWTH FACTOR; HEPATOCYTES; HUMANS; HYDROGEL; INDUCED PLURIPOTENT STEM CELLS; LIVER; LIVER FAILURE, ACUTE; LIVER REGENERATION; MALE; MALONDIALDEHYDE; MICE; MICE, INBRED BALB C; MICE, INBRED ICR; MICE, NUDE; REACTIVE OXYGEN SPECIES; THIOACETAMIDE;

EID: 84927158955     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368915X686986     Document Type: Article

References (50)

1. Atari, M.; Gil-Recio, C.; Fabregat, M.; Garcia-Fernandez, D.; Barajas, M.; Carrasco, M. A.; Jung, H. S.; Alfaro, F. H.; Casals, N.; Prosper, F.; Ferrés-Padró, E.; Giner, L. Dental pulp of the third molar: A new source of pluripotent-like stem cells. J. Cell Sci. 125(14):3343–3356; 2012.
2. Burr, A. W.; Toole, K.; Chapman, C.; Hines, J. E.; Burt, A. D. Anti-hepatocyte growth factor antibody inhibits hepatocyte proliferation during liver regeneration. J. Pathol. 185(3): 298–302; 1998.
3. Chen, G.; Hoffman, A. S. Graft copolymers that exhibit temperature-induced phase transitions over a wide range of pH. Nature 373(6509):49–52; 1995.
4. Chen, Y. C.; Hsu, H. S.; Chen, Y. W.; Tsai, T. H.; How, C. K.; Wang, C. Y.; Hung, S. C.; Chang, Y. L.; Tsai, M. L.; Lee, Y. Y.; Ku, H. H.; Chiou, S. H. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One 3(7):e2637; 2008.
5. Chen, Y. F.; Tseng, C. Y.; Wang, H. W.; Kuo, H. C.; Yang, V. W.; Lee, O. K. Rapid generation of mature hepatocytelike cells from human induced pluripotent stem cells by an efficient three-step protocol. Hepatology 55(4):1193–1203; 2012.
6. Chien, Y.; Liao, Y. W.; Liu, D. M.; Lin, H. L.; Chen, S. J.; Chen, H. L.; Peng, C. H.; Liang, C. M.; Mou, C. Y.; Chiou, S. H. Corneal repair by human corneal keratocytereprogrammed iPSCs and amphiphatic carboxymethyl-hexanoyl chitosan hydrogel. Biomaterials 33(32):8003–8016; 2012.
7. Chiou, S. H.; Kao, C. L.; Lin, H. T.; Tseng, W. S.; Liu, R. S.; Chung, C. F.; Ku, H. H.; Lin, C. P.; Wong, T. T. Monitoring the growth effect of xenotransplanted human medulloblastoma in an immunocompromised mouse model using in vitro and ex vivo green fluorescent protein imaging. Childs Nerv. Syst. 22(5):475–480; 2006.
8. Fulia, F.; Gitto, E.; Cuzzocrea, S.; Reiter, R. J.; Dugo, L.; Gitto, P.; Barberi, S.; Cordaro, S.; Barberi, I. Increased levels of malondialdehyde and nitrite/nitrate in the blood of asphyxiated newborns: Reduction by melatonin. J. Pineal Res. 31(4):343–349; 2001.
9. Garripelli, V. K.; Kim, J. K.; Namgung, R.; Kim, W. J.; Repka, M. A.; Jo, S. A novel thermosensitive polymer with pH-dependent degradation for drug delivery. Acta Biomater. 6(2):477–485; 2010.
10. Garripelli, V. K.; Kim, J. K.; Son, S.; Kim, W. J.; Repka, M. A.; Jo, S. Matrix metalloproteinase-sensitive thermogelling polymer for bioresponsive local drug delivery. Acta Biomater. 7(5):1984–1992; 2011.
11. Hirano, S.; Bless, D. M.; Nagai, H.; Rousseau, B.; Welham, N. V.; Montequin, D. W.; Ford, C. N. Growth factor therapy for vocal fold scarring in a canine model. Ann. Otol. Rhinol. Laryngol. 113(10):777–785; 2004.
12. Hughes, R. D.; Mitry, R. R.; Dhawan, A. Current status of hepatocyte transplantation. Transplantation 93(4):342–347; 2012.
13. Ishikawa, T.; Factor, V. M.; Marquardt, J. U.; Raggi, C.; Seo, D.; Kitade, M.; Conner, E. A.; Thorgeirsson, S. S. Hepatocyte growth factor/c-met signaling is required for stemcell- mediated liver regeneration in mice. Hepatology 55(4): 1215–1226; 2012.
14. Jeong, B.; Gutowska, A. Lessons from nature: Stimuliresponsive polymers and their biomedical applications. Trends Biotechnol. 20(7):305–311; 2002.
15. Jin, R.; Moreira Teixeira, L. S.; Dijkstra, P. J.; Karperien, M.; van Blitterswijk, C. A.; Zhong, Z. Y.; Feijen, J. Injectable chitosan-based hydrogels for cartilage tissue engineering. Biomaterials 30(13):2544–2551; 2009.
16. Kaur, N.; Nagpal, A. Extracted wisdom teeth: Preserve or discard??? Dent. Res. J. 10(3):408; 2013.
17. Kishimoto, Y.; Hirano, S.; Kitani, Y.; Suehiro, A.; Umeda, H.; Tateya, I.; Kanemaru, S.; Tabata, Y.; Ito, J. Chronic vocal fold scar restoration with hepatocyte growth factor hydrogel. Laryngoscope 120(1):108–113; 2010.
18. Kosai, K.; Matsumoto, K.; Nagata, S.; Tsujimoto, Y.; Nakamura, T. Abrogation of Fas-induced fulminant hepatic failure in mice by hepatocyte growth factor. Biochem. Biophys. Res. Commun. 244(3):683–690; 1998.
19. Lapasset, L.; Milhavet, O.; Prieur, A.; Besnard, E.; Babled, A.; Ait-Hamou, N.; Leschik, J.; Pellestor, F.; Ramirez, J. M.; De Vos, J.; Lehmann, S.; Lemaitre, J. M. Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes Dev. 25(21):2248–2253; 2011.
20. Lee, H. C.; Yin, P. H.; Lu, C. Y.; Chi, C. W.; Wei, Y. H. Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem. J. 348(2):425–432; 2000.
21. Lee, K.; Silva, E. A.; Mooney, D. J. Growth factor delivery-based tissue engineering: General approaches and a review of recent developments. J. R. Soc. Interface 8(55): 153–170; 2011.
22. Lee, P. Y.; Chien, Y.; Chiou, G. Y.; Chiou, C. H.; Tarng, D. C. Induced pluripotent stem cells without c-Myc attenuate acute kidney injury via down-regulating the signaling of oxidative stress and inflammation in ischemia- reperfusion rats. Cell Transplant. 21(12):2569–2585; 2012.
23. Lee, W. M. Acute liver failure. N. Engl. J. Med. 329(25): 1862–1872; 1993.
24. Li, H. Y.; Chien, Y.; Chen, Y. J.; Chen, S. F.; Chang, Y. L.; Chiang, C. H.; Jeng, S. Y.; Chang, C. M.; Wang, M. L.; Chen, L. K.; Hung, S. I.; Huo, T. I.; Lee, S. D.; Chiou, S. H. Reprogramming induced pluripotent stem cells in the absence of c-Myc for differentiation into hepatocyte-like cells. Biomaterials 32(26):5994–6005; 2011.
25. Li, X.; Kong, X.; Zhang, J.; Wang, Y.; Shi, S.; Guo, G.; Luo, F.; Zhao, X.; Wei, Y.; Qian, Z. A novel composite hydrogel based on chitosan and inorganic phosphate for local drug delivery of camptothecin nanocolloids. J. Pharm. Sci. 100(1):232–241; 2011.
26. Lin, T.; Ambasudhan, R.; Yuan, X.; Li, W.; Hilcove, S.; Abujarour, R.; Lin, X.; Hahm, H. S.; Hao, E.; Hayek, A.; Ding, S. A chemical platform for improved induction of human iPSCs. Nat. Methods 6(11):805–808; 2009.
27. Liu, T. Y.; Chen, S. Y.; Lin, Y. L.; Liu, D. M. Synthesis and characterization of amphiphatic carboxymethyl-hexanoyl chitosan hydrogel: Water-retention ability and drug encapsulation. Langmuir 22(23):9740–9745; 2006.
28. Matsuda, Y.; Matsumoto, K.; Yamada, A.; Ichida, T.; Asakura, H.; Komoriya, Y.; Nishiyama, E.; Nakamura, T. Preventive and therapeutic effects in rats of hepatocyte growth factor infusion on liver fibrosis/cirrhosis. Hepatology 26(1):81–89; 1997.
29. Matsumoto, K.; Nakamura, T. Hepatocyte growth factor (HGF) as a tissue organizer for organogenesis and regeneration. Biochem. Biophys. Res. Commun. 239(3):639–644; 1997.
30. Miura, M.; Gronthos, S.; Zhao, M.; Lu, B.; Fisher, L. W.; Robey, P. G.; Shi, S. SHED: Stem cells from human exfoliated deciduous teeth. Proc. Natl. Acad. Sci. USA 100(10): 5807–5812; 2003.
31. Mizuno, S.; Matsumoto, K.; Kurosawa, T.; Mizuno-Horikawa, Y.; Nakamura, T. Reciprocal balance of hepatocyte growth factor and transforming growth factor-beta 1 in renal fibrosis in mice. Kidney Int. 57(3):937–948; 2000.
32. Nakagawa, M.; Koyanagi, M.; Tanabe, K.; Takahashi, K.; Ichisaka, T.; Aoi, T.; Okita, K.; Mochiduki, Y.; Takizawa, N.; Yamanaka, S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat. Biotechnol. 26(1):101–106; 2008.
33. Nakamura, T.; Matsumoto, K.; Mizuno, S.; Sawa, Y.; Matsuda, H. Hepatocyte growth factor prevents tissue fibrosis, remodeling, and dysfunction in cardiomyopathic hamster hearts. Am. J. Physiol. Heart Circ. Physiol. 288(5): H2131–2139; 2005.
34. Nakamura, T.; Mizuno, S. The discovery of hepatocyte growth factor (HGF) and its significance for cell biology, life sciences and clinical medicine. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 86(6):588–610; 2010.
35. Nakamura, T.; Nawa, K.; Ichihara, A. Partial purification and characterization of hepatocyte growth factor from serum of hepatectomized rats. Biochem. Biophys. Res. Commun. 122(3):1450–1459; 1984.
36. Nosrat, I. V.; Widenfalk, J.; Olson, L.; Nosrat, C. A. Dental pulp cells produce neurotrophic factors, interact with trigeminal neurons in vitro, and rescue motoneurons after spinal cord injury. Dev. Biol. 238(1):120–132; 2001.
37. Nussler, A.; Konig, S.; Ott, M.; Sokal, E.; Christ, B.; Thasler, W.; Brulport, M.; Gabelein, G.; Schormann, W.; Schulze, M.; Ellis, E.; Kraemer, M.; Nocken, F.; Fleig, W.; Manns, M.; Strom, S. C.; Hengstler, J. G. Present status and perspectives of cell-based therapies for liver diseases. J. Hepatol. 45(1):144–159; 2006.
38. Oda, Y.; Yoshimura, Y.; Ohnishi, H.; Tadokoro, M.; Katsube, Y.; Sasao, M.; Kubo, Y.; Hattori, K.; Saito, S.; Horimoto, K.; Yuba, S.; Ohgushi, H. Induction of pluripotent stem cells from human third molar mesenchymal stromal cells. J. Biol. Chem. 285(38):29270–29278; 2010.
39. Ohno, T.; Hirano, S.; Kanemaru, S.; Yamashita, M.; Umeda, H.; Suehiro, A.; Tamura, Y.; Nakamura, T.; Ito, J.; Tabata, Y. Drug delivery system of hepatocyte growth factor for the treatment of vocal fold scarring in a canine model. Ann. Otol. Rhinol. Laryngol. 116(10):762–769; 2007.
40. Oyagi, S.; Hirose, M.; Kojima, M.; Okuyama, M.; Kawase, M.; Nakamura, T.; Ohgushi, H.; Yagi, K. Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats. J. Hepatol. 44(4):742–748; 2006.
41. Rashid, S. T.; Corbineau, S.; Hannan, N.; Marciniak, S. J.; Miranda, E.; Alexander, G.; Huang-Doran, I.; Griffin, J.; Ahrlund-Richter, L.; Skepper, J.; Semple, R.; Weber, A.; Lomas, D. A.; Vallier, L. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J. Clin. Invest. 120(9):3127–3136; 2010.
42. Sangiamsuntorn, K.; Wongkajornsilp, A.; Kasetsinsombat, K.; Duangsa-ard, S.; Nuntakarn, L.; Borwornpinyo, S.; Akarasereenont, P.; Limsrichamrern, S.; Hongeng, S. Upregulation of CYP 450s expression of immortalized hepatocyte-like cells derived from mesenchymal stem cells by enzyme inducers. BMC Biotechnol. 11:89; 2011.
43. Song, Z.; Cai, J.; Liu, Y.; Zhao, D.; Yong, J.; Duo, S.; Song, X.; Guo, Y.; Zhao, Y.; Qin, H.; Yin, X.; Wu, C.; Che, J.; Lu, S.; Ding, M.; Deng, H. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res. 19(11):1233–1242; 2009.
44. Ta, H. T.; Dass, C. R.; Dunstan, D. E. Injectable chitosan hydrogels for localised cancer therapy. J. Control. Release 126(3):205–216; 2008.
45. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872; 2007.
46. Tamaoki, N.; Takahashi, K.; Tanaka, T.; Ichisaka, T.; Aoki, H.; Takeda-Kawaguchi, T.; Iida, K.; Kunisada, T.; Shibata, T.; Yamanaka, S.; Tezuka, K. Dental pulp cells for induced pluripotent stem cell banking. J. Dent. Res. 89(8):773–778; 2010.
47. Tunon, M. J.; Alvarez, M.; Culebras, J. M.; Gonzalez-Gallego, J. An overview of animal models for investigating the pathogenesis and therapeutic strategies in acute hepatic failure. World J. Gastroenterol. 15(25):3086–3098; 2009.
48. Xia, J. L.; Dai, C.; Michalopoulos, G. K.; Liu, Y. Hepatocyte growth factor attenuates liver fibrosis induced by bile duct ligation. Am. J. Pathol. 168(5):1500–1512; 2006.
49. Yasuda, H.; Imai, E.; Shiota, A.; Fujise, N.; Morinaga, T.; Higashio, K. Antifibrogenic effect of a deletion variant of hepatocyte growth factor on liver fibrosis in rats. Hepatology 24(3):636–642; 1996.
50. Yu, L.; Ding, J. Injectable hydrogels as unique biomedical materials. Chem. Soc. Rev. 37(8):1473–1481; 2008.