Linoleic acid induces mouse embryonic stem cell proliferation via Ca 2+ /PKC, PI3K/Akt, and MAPKs

Cellular Physiology and Biochemistry

Volumn 23, Issue 1-3, 2009, Pages 53-64

  Kim, Min Hee ^a   Kim, Mi Ok ^b   Kim, Yun Hee ^b   Kim, Jin Sang ^a   Han, Ho Jae ^b  

^a Daegu University   (South Korea)

^b Chonnam National University   (South Korea)

Author keywords

Embryonic stem cell; Linoleic acid; MAPKs; PI3K Akt; PKC; Proliferation

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; BETA ACTIN; CALCIUM; CELL CYCLE PROTEIN; CYCLIN D1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN E; GLUCOSE; LINOLEIC ACID; MESSENGER RNA; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTEIN FOXD3; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C DELTA; PROTEIN KINASE C ZETA; STAUROSPORINE; THYMIDINE; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; EMBRYONIC STEM CELL; GENE EXPRESSION; GLUCONEOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 60549084725     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000204090     Document Type: Article

References (65)

1. Kotarsky K, Nilsson NE, Flodgren E, Owman C, Olde B: A human cell surface receptor activated by free fatty acids and thiazolidinedione drugs. Biochem Biophys Res Commun 2003;301:406-410.
2. Sessler AM, Ntambi JM: Polyunsaturated fatty acid regulation of gene expression. J Nutr 1998;128:923-926.
3. Iwata H, Inoue J, Kimura K, Kuge T, Kuwayama T, Monji Y: Comparison between the characteristics of follicular fluid and the developmental competence of bovine oocytes. Anim Reprod Sci 2006;91:215-223.
4. Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A: Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 2005;130:485-495.
5. Thomas MG, Bao B, Williams GL: Dietary fats varying in their fatty acid composition differentially influence follicular growth in cows fed isoenergetic diets. J Anim Sci 1997;75:2512-2519.
6. Thangavelu G, Colazo MG, Ambrose DJ, Oba M, Okine EK, Dyck MK: Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows. Theriogenology 2007;68:949-957.
7. Das UN: Biological significance of essential fatty acids. J Assoc Physicians India 2006;54:309-319.
8. Mashek DG, Grummer RR: Effects of long chain fatty acids on lipid and glucose metabolism in monolayer cultures of bovine hepatocytes. J Dairy Sci 2003;86:2390-2396.
9. Wyne KL: Free fatty acids and type 2 diabetes mellitus. Am J Med 2003;115 Suppl 8A:29S-36S.
10. Collins QF, Xiong Y, Lupo EG, Jr., Liu HY, Cao W: p38 Mitogen-activated protein kinase mediates free fatty acid-induced gluconeogenesis in hepatocytes. J Biol Chem 2006;281:24336-24344.
11. Milligan G, Stoddart LA, Brown AJ: G protein-coupled receptors for free fatty acids. Cell Signal 2006;18:1360-1365.
12. Covington DK, Briscoe CA, Brown AJ, Jayawickreme CK: The G-protein-coupled receptor 40 family (GPR40-GPR43) and its role in nutrient sensing. Biochem Soc Trans 2006;34:770-773.
13. Sawzdargo M, George SR, Nguyen T, Xu S, Kolakowski LF, O'Dowd BF: A cluster of four novel human G protein-coupled receptor genes occurring in close proximity to CD22 gene on chromosome 19q13.1. Biochem Biophys Res Commun 1997;239:543-547.
14. Ma D, Lu L, Boneva NB, Warashina S, Kaplamadzhiev DB, Mori Y, Nakaya MA, Kikuchi M, Tonchev AB, Okano H, Yamashima T: Expression of free fatty acid receptor GPR40 in the neurogenic niche of adult monkey hippocampus. Hippocampus 2008;18:326-333.
15. Brown AJ, Jupe S, Briscoe CP: A family of fatty acid binding receptors. DNA Cell Biol 2005;24:54-61.
16. Guasch G, Fuchs E: Mice in the world of stem cell biology. Nat Genet 2005;37:1201-1206.
17. Chase LG, Firpo MT: Development of serum-free culture systems for human embryonic stem cells. Curr Opin Chem Biol 2007;11:367-372.
18. Gruen L, Grabel L: Concise review: scientific and ethical roadblocks to human embryonic stem cell therapy. Stem Cells 2006;24:2162-2169.
19. Chen CH, Ho ML, Chang JK, Hung SH, Wang GJ: Green tea catechin enhances osteogenesis in a bone marrow mesenchymal stem cell line. Osteoporos Int 2005;16:2039-2045.
20. Zhang E, Li X, Zhang S, Chen L, Zheng X: Cell cycle synchronization of embryonic stem cells: effect of serum deprivation on the differentiation of embryonic bodies in vitro. Biochem Biophys Res Commun 2005;333:1171-1177.
21. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
22. Chung JW, Kim GY, Mun YC, Ahn JY, Seong CM, Kim JH: Leukotriene B4 pathway regulates the fate of the hematopoietic stem cells. Exp Mol Med 2005;37:45-50.
23. Zhu Y, Schwarz S, Ahlemeyer B, Grzeschik S, Klumpp S, Krieglstein J: Oleic acid causes apoptosis and dephosphorylates Bad. Neurochem Int 2005;46:127-135.
24. Fang IM, Yang CH, Yang CM, Chen MS: Linoleic acid-induced expression of inducible nitric oxide synthase and cyclooxygenase II via p42/44 mitogen-activated protein kinase and nuclear factor-κB pathway in retinal pigment epithelial cells. Exp Eye Res 2007;85:667-677.
25. Tikhonova IG, Sum CS, Neumann S, Thomas CJ, Raaka BM, Costanzi S, Gershengorn MC: Bidirectional, Iterative Approach to the Structural Delineation of the Functional "Chemoprint" in GPR40 for Agonist Recognition. J Med Chem 2007;50:2981-2989.
26. Briscoe CP, Tadayyon M, Andrews JL, Benson WG, Chambers JK, Eilert MM, Ellis C, Elshourbagy NA, Goetz AS, Minnick DT, Murdock PR, Sauls HR, Jr., Shabon U, Spinage LD, Strum JC, Szekeres PG, Tan KB, Way JM, Ignar DM, Wilson S, Muir AI: The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. J Biol Chem 2003;278:11303-11311.
27. Wettschureck N, Offermanns S: Mammalian G proteins and their cell type specific functions. Physiol Rev 2005;85:1159-1204.
28. Lee DK, George SR, O'Dowd BF: Continued discovery of ligands for G protein-coupled receptors. Life Sci 2003;74:293-297.
29. Heo JS, Han HJ: ATP stimulates mouse embryonic stem cell proliferation via protein kinase C, phosphatidylinositol 3-kinase/Akt, and mitogen-activated protein kinase signaling pathways. Stem Cells 2006;24:2637-2648.
30. 2+ /PKC as well as EGF receptor-dependent PI3K/Akt/mTOR/ p70S6K1 signal pathways in mouse embryonic stem cells. J Cell Physiol 2007;211:618-629.
31. Greco S, Muscella A, Elia MG, Salvatore P, Storelli C, Mazzotta A, Manca C, Marsigliante S: Angiotensin II activates extracellular signal regulated kinases via protein kinase C and epidermal growth factor receptor in breast cancer cells. J Cell Physiol 2003;196:370-377.
32. Zhao Y, Liu J, Li L, Liu L, Wu L: Role of Ras/PKC ζ/MEK/ERK1/2 signaling pathway in angiotensin II-induced vascular smooth muscle cell proliferation. Regul Pept 2005;128:43-50.
33. Yano S, Tokumitsu H, Soderling TR: Calcium promotes cell survival through CaM-K kinase activation of the proteinkinase-B pathway. Nature 1998;396:584-587.
34. Rozengurt E: Mitogenic signaling pathways induced by G protein-coupled receptors. J Cell Physiol 2007;213:589-602.
35. Takahashi K, Murakami M, Yamanaka S: Role of the phosphoinositide 3-kinase pathway in mouse embryonic stem (ES) cells. Biochem Soc Trans 2005;33:1522-1525.
36. Dugourd C, Gervais M, Corvol P, Monnot C: Akt is a major downstream target of PI3-kinase involved in angiotensin II-induced proliferation. Hypertension 2003;41:882-890.
37. Stabile E, Zhou YF, Saji M, Castagna M, Shou M, Kinnaird TD, Baffour R, Ringel MD, Epstein SE, Fuchs S: Akt controls vascular smooth muscle cell proliferation in vitro and in vivo by delaying G1/S exit. Circ Res 2003;93:1059-1065.
38. Hardy S, Langelier Y, Prentki M: Oleate activates phosphatidylinositol 3-kinase and promotes proliferation and reduces apoptosis of MDA-MB-231 breast cancer cells, whereas palmitate has opposite effects. Cancer Res 2000;60:6353-6358.
39. Yun MR, Lee JY, Park HS, Heo HJ, Park JY, Bae SS, Hong KW, Sung SM, Kim CD: Oleic acid enhances vascular smooth muscle cell proliferation via phosphatidylinositol 3-kinase/Akt signaling pathway. Pharmacol Res 2006;54:97-102.
40. Rao GN, Alexander RW, Runge MS: Linoleic acid and its metabolites, hydroperoxyoctadecadienoic acids, stimulate c-Fos, c-Jun, and c-Myc mRNA expression, mitogen-activated protein kinase activation, and growth in rat aortic smooth muscle cells. J Clin Invest 1995;96:842-847.
41. Katsuma S, Hatae N, Yano T, Ruike Y, Kimura M, Hirasawa A, Tsujimoto G: Free fatty acids inhibit serum deprivation-induced apoptosis through GPR120 in a murine enteroendocrine cell line STC-1. J Biol Chem 2005;280:19507-19515.
42. Hennig B, Lei W, Arzuaga X, Ghosh DD, Saraswathi V, Toborek M: Linoleic acid induces proinflammatory events in vascular endothelial cells via activation of PI3K/Akt and ERK1/2 signaling. J Nutr Biochem 2006;17:766-772.
43. Lopez-Ilasaca M, Crespo P, Pellici PG, Gutkind JS, Wetzker R: Linkage of G protein-coupled receptors to the MAPK signaling pathway through PI 3-kinase γ. Science 1997;275:394-397.
44. Hawes BE, Luttrell LM, van Biesen T, Lefkowitz RJ: Phosphatidylinositol 3-kinase is an early intermediate in the G βγ-mediated mitogen-activated protein kinase signaling pathway. J Biol Chem 1996;271:12133-12136.
45. Lam TK, Carpentier A, Lewis GF, van de Werve G, Fantus IG, Giacca A: Mechanisms of the free fatty acid-induced increase in hepatic glucose production. Am J Physiol Endocrinol Metab 2003;284:E863-873.
46. Antras-Ferry J, Le Bigot G, Robin P, Robin D, Forest C: Stimulation of phosphoenolpyruvate carboxykinase gene expression by fatty acids. Biochem Biophys Res Commun 1994;203:385-391.
47. Bizeau ME, Hazel JR: Dietary fat type alters glucose metabolism in isolated rat hepatocytes. J Nutr Biochem 1999;10:709-715.
48. Lam TK, Pocai A, Gutierrez-Juarez R, Obici S, Bryan J, Aguilar-Bryan L, Schwartz GJ, Rossetti L: Hypothalamic sensing of circulating fatty acids is required for glucose homeostasis. Nat Med 2005;11:320-327.
49. Barthel A, Schmoll D: Novel concepts in insulin regulation of hepatic gluconeogenesis. Am J Physiol Endocrinol Metab 2003;285:E685-692.
50. Yanez AJ, Nualart F, Droppelmann C, Bertinat R, Brito M, Concha, II, Slebe JC: Broad expression of fructose-1,6-bisphosphatase and phosphoenolpyruvate carboxykinase provide evidence for gluconeogenesis in human tissues other than liver and kidney. J Cell Physiol 2003;197:189-197.
51. Navarrete Santos A, Ramin N, Tonack S, Fischer B: Cell lineage-specific signaling of insulin and insulin-like growth factor I in rabbit blastocysts. Endocrinology 2008;149:515-524.
52. Han HJ, Heo JS, Lee YJ: Estradiol-17β stimulates proliferation of mouse embryonic stem cells: involvement of MAPKs and CDKs as well as protooncogenes. Am J Physiol Cell Physiol 2006;290:C1067-1075.
53. Jirmanova L, Afanassieff M, Gobert-Gosse S, Markossian S, Savatier P: Differential contributions of ERK and PI3-kinase to the regulation of cyclin D1 expression and to the control of the G1/S transition in mouse embryonic stem cells. Oncogene 2002;21:5515-5528.
54. Shen F, Fan X, Liu B, Jia X, Du H, You B, Ye M, Huang C, Shi X: Overexpression of cyclin D1-CDK4 in silica-induced transformed cells is due to activation of ERKs, JNKs/AP-1 pathway. Toxicol Lett 2006;160:185-195.
55. Mirza AM, Gysin S, Malek N, Nakayama K, Roberts JM, McMahon M: Cooperative regulation of the cell division cycle by the protein kinases RAF and AKT. Mol Cell Biol 2004;24:10868-10881.
56. Murata M, Kaji H, Iida K, Okimura Y, Chihara K: Dual action of eicosapentaenoic acid in hepatoma cells: up-regulation of metabolic action of insulin and inhibition of cell proliferation. J Biol Chem 2001;276:31422-31428.
57. Roche E, Buteau J, Aniento I, Reig JA, Soria B, Prentki M: Palmitate and oleate induce the immediate-early response genes c-fos and nur-77 in the pancreatic β-cell line INS-1. Diabetes 1999;48:2007-2014.
58. 2+ in the regulation of gluconeogenesis. Metabolism 1996;45:389-403.
59. Grimaldi PA: Peroxisome proliferator-activated receptors as sensors of fatty acids and derivatives. Cell Mol Life Sci 2007;64:2459-2464.
60. 2 and peroxisome proliferator-activated receptor δ promote mouse embryonic stem cell proliferation. Stem Cells 2008;26:745-755.
61. Xu J, Xiao G, Trujillo C, Chang V, Blanco L, Joseph SB, Bassilian S, Saad MF, Tontonoz P, Lee WN, Kurland IJ: Peroxisome proliferator-activated receptor α (PPAR α) influences substrate utilization for hepatic glucose production. J Biol Chem 2002;277:50237-50244.
62. Harrison RA: The detection of hexokinase, glucosephosphate isomerase and phosphoglucomutase activities in polyacrylamide gels after electrophoresis: a novel method using immobilized glucose 6-phosphate dehydrogenase. Anal Biochem 1974;61:500-507.
63. Silletti S, Raz A: Autocrine motility factor is a growth factor. Biochem Biophys Res Commun 1993;194:446-457.
64. Funasaka T, Hu H, Hogan V, Raz A: Downregulation of phosphoglucose isomerase/ autocrine motility factor expression sensitizes human fibrosarcoma cells to oxidative stress leading to cellular senescence. J Biol Chem 2007;282:36362-36369.
65. Tsutsumi S, Hogan V, Nabi IR, Raz A: Overexpression of the autocrine motility factor/phosphoglucose isomerase induces transformation and survival of NIH-3T3 fibroblasts. Cancer Res 2003;63:242-249.