Nicotinamide overcomes pluripotency deficits and reprogramming barriers

Stem Cells

Volumn 31, Issue 6, 2013, Pages 1121-1135

  Son, Myung Jin ^a,b   Son, Mi Young ^a   Seol, Binna ^a   Kim, Min Jeong ^a,b   Yoo, Chae Hwa ^a   Han, Myung Kwan ^c   Cho, Yee Sook ^a,b  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

^c Chonbuk National University Medical School   (South Korea)

Author keywords

Human embryonic stem cell; Human induced pluripotent stem cell; NAD+; Nicotinamide; Pluripotency; Reprogramming

Indexed keywords

DAPORINAD; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINIC ACID; PROTEIN P16; PROTEIN P21; PROTEIN P53; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CELL AGING; CELL KINETICS; CELL LINE; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTRACELLULAR SIGNALING; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; SOMATIC CELL;

APOPTOSIS; CELL LINE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DOWN-REGULATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KINETICS; MEMBRANE POTENTIAL, MITOCHONDRIAL; NAD; NEOPLASM PROTEINS; NIACIN; NIACINAMIDE; NUCLEAR REPROGRAMMING; OXIDATIVE STRESS; PLURIPOTENT STEM CELLS; REACTIVE OXYGEN SPECIES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84877960769     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1368     Document Type: Article

References (58)

1. Burkle A. Physiology and pathophysiology of poly(ADP-ribosyl)ation. Bioessays 2001;23:795-806. (Pubitemid 32901331)
2. Ghosh S, George S, Roy U et al. NAD: A master regulator of transcription. Biochim Biophys Acta 2010;1799:681-693.
3. Yang H, Yang T, Baur JA et al. Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 2007;130:1095-1107. (Pubitemid 47410271)
4. Lin SJ, Kaeberlein M, Andalis AA et al. Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 2002;418:344-348. (Pubitemid 34790687)
5. Cohen HY, Miller C, Bitterman KJ et al. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 2004;305:390-392. (Pubitemid 38938153)
6. Houtkooper RH, Canto C, Wanders RJ et al. The secret life of NAD+: An old metabolite controlling new metabolic signaling pathways. Endocr Rev 2010;31:194-223.
7. Belenky P, Racette FG, Bogan KL et al. Nicotinamide riboside promotes Sir2 silencing and extends lifespan via Nrk and Urh1/Pnp1/Meu1 pathways to NAD+. Cell 2007;129:473-484. (Pubitemid 46660969)
8. Bogan KL, Brenner C. Nicotinic acid, nicotinamide, and nicotinamide riboside: A molecular evaluation of NAD+ precursor vitamins in human nutrition. Annu Rev Nutr 2008;28:115-130.
9. Yang T, Sauve AA. NAD metabolism and sirtuins: Metabolic regulation of protein deacetylation in stress and toxicity. AAPS J 2006;8:E632-E643. (Pubitemid 44644162)
10. Calvanese V, Fraga MF. SirT1 brings stemness closer to cancer and aging. Aging (Albany NY) 2011;3:162-167.
11. Vaca P, Berna G, Araujo R et al. Nicotinamide induces differentiation of embryonic stem cells into insulin-secreting cells. Exp Cell Res 2008;314:969-974.
12. Vaca P, Berna G, Martin F et al. Nicotinamide induces both proliferation and differentiation of embryonic stem cells into insulin-producing cells. Transplant Proc 2003;35:2021-2023. (Pubitemid 37093799)
13. Bhansali SG, Brazeau DA, Sonee M et al. Nicotinamide prevents apoptosis in human cortical neuronal cells. Toxicol Mech Methods 2006;16:173-180.
14. Skokowa J, Lan D, Thakur BK et al. NAMPT is essential for the G-CSF-induced myeloid differentiation via a NAD(+)-sirtuin-1-dependent pathway. Nat Med 2009;15:151-158.
15. Li Y, He X, He J et al. Nicotinamide phosphoribosyltransferase (Nampt) affects the lineage fate determination of mesenchymal stem cells: A possible cause for reduced osteogenesis and increased adipogenesis in older individuals. J Bone Miner Res 2011;26:2656-2664.
16. van der Veer E, Ho C, O'Neil C et al. Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J Biol Chem 2007;282:10841-10845. (Pubitemid 47100731)
17. Gao F, Kwon SW, Zhao Y et al. PARP1 poly(ADP-ribosyl)ates Sox2 to control Sox2 protein levels and FGF4 expression during embryonic stem cell differentiation. J Biol Chem 2009;284:22263-22273.
18. Chen HP, Denicola M, Qin X et al. HDAC inhibition promotes cardiogenesis and the survival of embryonic stem cells through proteasome-dependent pathway. J Cell Biochem 2011;112:3246-3255.
19. Varum S, Rodrigues AS, Moura MB et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. Plos One 2011;6:e20914.
20. Folmes CD, Nelson TJ, Martinez-Fernandez A et al. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 2011;14:264-271.
21. Xu C, Inokuma MS, Denham J et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001;19:971-974. (Pubitemid 32947578)
22. Yao S, Chen S, Clark J et al. Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions. Proc Natl Acad Sci USA 2006;103:6907-6912.
23. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872. (Pubitemid 350138099)
24. Luo X, Kraus WL. On PAR with PARP: Cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 2012;26:417-432.
25. Banito A, Rashid ST, Acosta JC et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 2009;23:2134-2139.
26. Kawamura T, Suzuki J, Wang YV et al. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 2009;460:1140-1144.
27. Utikal J, Polo JM, Stadtfeld M et al. Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 2009;460:1145-1148.
28. Xu C, Rosler E, Jiang J et al. Basic fibroblast growth factor supports undifferentiated human embryonic stem cell growth without conditioned medium. Stem Cells 2005;23:315-323. (Pubitemid 40404450)
29. Xu RH, Peck RM, Li DS et al. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2005;2:185-190. (Pubitemid 41122125)
30. Beattie GM, Lopez AD, Bucay N et al. Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers. Stem Cells 2005;23:489-495. (Pubitemid 40478488)
31. Amit M, Shariki C, Margulets V et al. Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod 2004;70:837-845. (Pubitemid 38233724)
32. Pebay A, Wong RC, Pitson SM et al. Essential roles of sphingosine-1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells. Stem Cells 2005;23:1541-1548. (Pubitemid 41741003)
33. Pyle AD, Lock LF, Donovan PJ. Neurotrophins mediate human embryonic stem cell survival. Nat Biotechnol 2006;24:344-350. (Pubitemid 43372159)
34. Son MY, Kim MJ, Yu K et al. Involvement of neuropeptide Y and its Y1 and Y5 receptors in maintaining self-renewal and proliferation of human embryonic stem cells. J Cell Mol Med 2011;15:152-165.
35. Huangfu D, Osafune K, Maehr R et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 2008;26:1269-1275.
36. Lin T, Ambasudhan R, Yuan X et al. A chemical platform for improved induction of human iPSCs. Nat Methods 2009;6:805-808.
37. Ezashi T, Das P, Roberts RM. Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 2005;102:4783-4788. (Pubitemid 40471531)
38. Zachar V, Prasad SM, Weli SC et al. The effect of human embryonic stem cells (hESCs) long-term normoxic and hypoxic cultures on the maintenance of pluripotency. In Vitro Cell Dev Anim 2010;46:276-283.
39. Panopoulos AD, Ruiz S, Yi F et al. Rapid and highly efficient generation of induced pluripotent stem cells from human umbilical vein endothelial cells. Plos One 2011;6:e19743.
40. Belenky P, Bogan KL, Brenner C. NAD+ metabolism in health and disease. Trends Biochem Sci 2007;32:12-19.
41. Jackson TM, Rawling JM, Roebuck BD et al. Large supplements of nicotinic acid and nicotinamide increase tissue NAD+ and poly(ADP-ribose) levels but do not affect diethylnitrosamine-induced altered hepatic foci in Fischer-344 rats. J Nutr 1995;125:1455-1461.
42. Jacobson EL, Dame AJ, Pyrek JS et al. Evaluating the role of niacin in human carcinogenesis. Biochimie 1995;77:394-398.
43. Collins PB, Chaykin S. The management of nicotinamide and nicotinic acid in the mouse. J Biol Chem 1972;247:778-783.
44. Bai L, Pang WJ, Yang YJ et al. Modulation of Sirt1 by resveratrol and nicotinamide alters proliferation and differentiation of pig preadipocytes. Mol Cell Biochem 2008;307:129-140. (Pubitemid 350238655)
45. Otonkoski T, Beattie GM, Mally MI et al. Nicotinamide is a potent inducer of endocrine differentiation in cultured human fetal pancreatic cells. J Clin Invest 1993;92:1459-1466. (Pubitemid 23273925)
46. Marion RM, Strati K, Li H et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009;460:1149-1153.
47. Li H, Collado M, Villasante A et al. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009;460:1136-1139.
48. Vazquez-Martin A, Vellon L, Quiros PM et al. Activation of AMP-activated protein kinase (AMPK) provides a metabolic barrier to reprogramming somatic cells into stem cells. Cell cycle 2012;11.
49. Chen M, Zhang H, Wu J et al. Promotion of the induction of cell pluripotency through metabolic remodeling by thyroid hormone triiodothyronine-activated PI3K/AKT signal pathway. Biomaterials 2012;33:5514-5523.
50. Kang HT, Lee HI, Hwang ES. Nicotinamide extends replicative lifespan of human cells. Aging Cell 2006;5:423-436. (Pubitemid 44322538)
51. Matuoka K, Chen KY, Takenawa T. Rapid reversion of aging phenotypes by nicotinamide through possible modulation of histone acetylation. Cell Mol Life Sci 2001;58:2108-2116. (Pubitemid 34016979)
52. Tait SW, Green DR. Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010;11:621-632.
53. Miura T, Mattson MP, Rao MS. Cellular lifespan and senescence signaling in embryonic stem cells. Aging Cell 2004;3:333-343. (Pubitemid 40246703)
54. Houtkooper RH, Pirinen E, Auwerx J. Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 2012;13:225-238.
55. Garten A, Petzold S, Korner A et al. Nampt: Linking NAD biology, metabolism and cancer. Trends Endocrinol Metab 2009;20:130-138.
56. de Murcia JM, Niedergang C, Trucco C et al. Requirement of poly(-ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc Natl Acad Sci USA 1997;94:7303-7307. (Pubitemid 27345310)
57. Virag L, Salzman AL, Szabo C. Poly(ADP-ribose) synthetase activation mediates mitochondrial injury during oxidant-induced cell death. J Immunol 1998;161:3753-3759.
58. Doege CA, Inoue K, Yamashita T et al. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 2012;488:652-655.