Lysophosphatidic acid acts as a nutrient-derived developmental cue to regulate early hematopoiesis

EMBO Journal

Volumn 33, Issue 12, 2014, Pages 1383-1396

  Li, Haisen ^a   Yue, Rui ^a,b   Wei, Bin ^a   Gao, Ge ^c   Du, Jiulin ^d   Pei, Gang ^a,e  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c PEKING UNIVERSITY   (China)

^d Chinese Academy of Sciences   (China)

^e TONGJI UNIVERSITY   (China)

Author keywords

embryonic stem cell; hemangioblast; hematopoiesis; LPA; zebrafish

Indexed keywords

AUTOTAXIN; BETA ACTIN; CMYB PROTEIN; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHATIDIC ACID RECEPTOR 2; LYSOPHOSPHATIDIC ACID RECEPTOR 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE A2; PROTEIN KINASE B; RAC1 PROTEIN; SMAD PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; COLONY FORMING CELL; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; HEMANGIOBLAST; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ZEBRA FISH;

EMBRYONIC STEM CELL; HEMANGIOBLAST; HEMATOPOIESIS; LPA; ZEBRAFISH;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; EMBRYONIC DEVELOPMENT; FLOW CYTOMETRY; HEMANGIOBLASTS; HEMATOPOIESIS; IN SITU HYBRIDIZATION; LYSOPHOSPHOLIPIDS; MICE; MICROSCOPY, FLUORESCENCE; PHOSPHORIC DIESTER HYDROLASES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, LYSOPHOSPHATIDIC ACID; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 84903310574     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201387594     Document Type: Article

References (63)

1. Allende ML, Yamashita T, Proia RL, (2003) G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102: 3665-3667
2. Anliker B, Chun J, (2004) Lysophospholipid G protein-coupled receptors. J Biol Chem 279: 20555-20558
3. Birgbauer E, Chun J, (2006) New developments in the biological functions of lysophospholipids. Cell Mol Life Sci 63: 2695-2701
4. Chaurio RA, Janko C, Munoz LE, Frey B, Herrmann M, Gaipl US, (2009) Phospholipids: key players in apoptosis and immune regulation. Molecules 14: 4892-4914
5. Chiang CL, Chen SS, Lee SJ, Tsao KC, Chu PL, Wen CH, Hwang SM, Yao CL, Lee H, (2011) Lysophosphatidic acid induces erythropoiesis through activating lysophosphatidic acid receptor 3. Stem Cells 29: 1763-1773
6. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G, (1998) A common precursor for hematopoietic and endothelial cells. Development 125: 725-732
7. Contos JJ, Fukushima N, Weiner JA, Kaushal D, Chun J, (2000) Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc Natl Acad Sci USA 97: 13384-13389
8. Cook BD, Liu S, Evans T, (2011) Smad1 signaling restricts hematopoietic potential after promoting hemangioblast commitment. Blood 117: 6489-6497
9. Damert A, Miquerol L, Gertsenstein M, Risau W, Nagy A, (2002) Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development 129: 1881-1892
10. Eilken HM, Nishikawa S, Schroeder T, (2009) Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457: 896-900
11. Ema M, Faloon P, Zhang WJ, Hirashima M, Reid T, Stanford WL, Orkin S, Choi K, Rossant J, (2003) Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev 17: 380-393
12. Estivill-Torrus G, Llebrez-Zayas P, Matas-Rico E, Santin L, Pedraza C, De Diego I, Del Arco I, Fernandez-Llebrez P, Chun J, De Fonseca FR, (2008) Absence of LPA1 signaling results in defective cortical development. Cereb Cortex 18: 938-950
13. Fehling HJ, Lacaud G, Kubo A, Kennedy M, Robertson S, Keller G, Kouskoff V, (2003) Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130: 4217-4227
14. Feng XH, Derynck R, (2005) Specificity and versatility in TGF-beta signaling through Smads. Annu Rev Cell Dev Biol 21: 659-693
15. Ferry G, Giganti A, Cogé F, Bertaux F, Thiam K, Boutin JA, (2007) Functional invalidation of the autotaxin gene by a single amino acid mutation in mouse is lethal. FEBS Lett 581: 3572-3578
16. Fisher MC, Zeisel SH, Mar MH, Sadler TW, (2002) Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro. Faseb J 16: 619-621
17. Freyer C, Renfree MB, (2009) The mammalian yolk sac placenta. J Exp Zool B Mol Dev Evol 312: 545-554
18. Fukushima N, Kimura Y, Chun J, (1998) A single receptor encoded by vzg-1/lpA1/edg-2 couples to G proteins and mediates multiple cellular responses to lysophosphatidic acid. Proc Natl Acad Sci USA 95: 6151-6156
19. Fukushima N, Ishii I, Contos JJ, Weiner JA, Chun J, (2001) Lysophospholipid receptors. Annu Rev Pharmacol Toxicol 41: 507-534
20. Gadue P, Huber TL, Paddison PJ, Keller GM, (2006) Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci USA 103: 16806-16811
21. Gaengel K, Niaudet C, Hagikura K, Laviña B, Muhl L, Hofmann JJ, Ebarasi L, Nyström S, Rymo S, Chen LL, Pang MF, Jin Y, Raschperger E, Roswall P, Schulte D, Benedito R, Larsson J, Hellström M, Fuxe J, Uhlén P, et al, (2012) The Sphingosine-1-Phosphate Receptor S1PR1 Restricts Sprouting Angiogenesis by Regulating the Interplay between VE-Cadherin and VEGFR2. Dev Cell 23: 587-599
22. Gering M, Yamada Y, Rabbitts TH, Patient RK, (2003) Lmo2 and SCL/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1. Development 130: 6187-6199
23. Guo F, Jen KL, (1995) High-fat feeding during pregnancy and lactation affects offspring metabolism in rats. Physiol Behav 57: 681-686
24. Hailesellasse Sene K, Porter CJ, Palidwor G, Perez-Iratxeta C, Muro EM, Campbell PA, Rudnicki MA, Andrade-Navarro MA, (2007) Gene function in early mouse embryonic stem cell differentiation. BMC Genomics 8: 85
25. Hales CN, Barker DJ, (2001) The thrifty phenotype hypothesis. Br Med Bull 60: 5-20
26. Hao J, Ho JN, Lewis JA, Karim KA, Daniels RN, Gentry PR, Hopkins CR, Lindsley CW, Hong CC, (2010) In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem Biol 5: 245-253
27. Hochman E, Kinston S, Harmelin A, Gottgens B, Izraeli S, (2006) The SCL 3′ enhancer responds to Hedgehog signaling during hemangioblast specification. Exp Hematol 34: 1643-1650
28. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G, (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432: 625-630
29. Jin X, Yin J, Kim SH, Sohn YW, Beck S, Lim YC, Nam DH, Choi YJ, Kim H, (2011) EGFR-AKT-Smad signaling promotes formation of glioma stem-like cells and tumor angiogenesis by ID3-driven cytokine induction. Cancer Res 71: 7125-7134
30. Johansson BM, Wiles MV, (1995) Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol Cell Biol 15: 141-151
31. Kennedy M, Firpo M, Choi K, Wall C, Robertson S, Kabrun N, Keller G, (1997) A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 386: 488-493
32. Khan IY, Dekou V, Douglas G, Jensen R, Hanson MA, Poston L, Taylor PD, (2005) A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol 288: R127-R133
33. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310
34. Kissa K, Murayama E, Zapata A, Cortes A, Perret E, Machu C, Herbomel P, (2008) Live imaging of emerging hematopoietic stem cells and early thymus colonization. Blood 111: 1147-1156
35. Koike S, Keino-Masu K, Ohto T, Sugiyama F, Takahashi S, Masu M, (2009) Autotaxin/Lysophospholipase D-mediated Lysophosphatidic Acid Signaling Is Required to Form Distinctive Large Lysosomes in the Visceral Endoderm Cells of the Mouse Yolk Sac. J Biol Chem 284: 33561-33570
36. Lai SL, Yao WL, Tsao KC, Houben AJ, Albers HM, Ovaa H, Moolenaar WH, Lee SJ, (2012) Autotaxin/Lpar3 signaling regulates Kupffer's vesicle formation and left-right asymmetry in zebrafish. Development 139: 4439-4448
37. Lancrin C, Sroczynska P, Stephenson C, Allen T, Kouskoff V, Lacaud G, (2009) The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 457: 892-895
38. Lee Z, Cheng CT, Zhang H, Subler MA, Wu J, Mukherjee A, Windle JJ, Chen CK, Fang X, (2008) Role of LPA4/p2y9/GPR23 in negative regulation of cell motility. Mol Biol Cell 19: 5435-5445
39. Liu Y, Wada R, Yamashita T, Mi Y, Deng CX, Hobson JP, Rosenfeldt HM, Nava VE, Chae SS, Lee MJ, Liu CH, Hla T, Spiegel S, Proia RL, (2000) Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J Clin Invest 106: 951-961
40. Liu F, Walmsley M, Rodaway A, Patient R, (2008) Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr Biol 18: 1234-1240
41. Lugus JJ, Chung YS, Mills JC, Kim SI, Grass J, Kyba M, Doherty JM, Bresnick EH, Choi K, (2007) Gata2 functions at multiple steps in hemangioblast development and differentiation. Development 134: 393-405
42. McKinney-Freeman SL, Naveiras O, Daley GQ, (2008) Isolation of hematopoietic stem cells from mouse embryonic stem cells. Curr Protoc Stem Cell Biol 4: 1F.3.1-1F.3.10
43. van Meeteren LA, Ruurs P, Stortelers C, Bouwman P, van Rooijen MA, Pradère JP, Pettit TR, Wakelam MJ, Saulnier-Blache JS, Mummery CL, Moolenaar WH, Jonkers J, (2006) Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol Cell Biol 26: 5015-5022
44. Mills GB, Moolenaar WH, (2003) The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 3: 582-591
45. Noble RC, Moore JH, (1967) The transport of phospholipids from the yolk to the yolk-sac membrane during the development of the chick embryo. Can J Biochem 45: 1125-1133
46. Nostro MC, Cheng X, Keller GM, Gadue P, (2008) Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2: 60-71
47. Orkin SH, Zon LI, (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132: 631-644
48. Park C, Afrikanova I, Chung YS, Zhang WJ, Arentson E, Fong G, Rosendahl A, Choi K, (2004) A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 131: 2749-2762
49. Park C, Lugus JJ, Choi K, (2005) Stepwise commitment from embryonic stem to hematopoietic and endothelial cells. Curr Top Dev Biol 66: 1-36
50. Qian F, Zhen F, Xu J, Huang M, Li W, Wen Z, (2007) Distinct functions for different scl isoforms in zebrafish primitive and definitive hematopoiesis. PLoS Biol 5: e132
51. Rai V, Toure F, Chitayat S, Pei R, Song F, Li Q, Zhang J, Rosario R, Ramasamy R, Chazin WJ, Schmidt AM, (2012) Lysophosphatidic acid targets vascular and oncogenic pathways via RAGE signaling. J Exp Med 209: 2339-2350
52. Sachinidis A, Gissel C, Nierhoff D, Hippler-Altenburg R, Sauer H, Wartenberg M, Hescheler J, (2003) Identification of plateled-derived growth factor-BB as cardiogenesis- inducing factor in mouse embryonic stem cells under serum-free conditions. Cell Physiol Biochem 13: 423-429
53. Schmitz G, Ruebsaamen K, (2009) Metabolism and atherogenic disease association of lysophosphatidylcholine. Atherosclerosis 208: 10-18
54. Soderberg SS, Karlsson G, Karlsson S, (2009) Complex and context dependent regulation of hematopoiesis by TGF-beta superfamily signaling. Ann N Y Acad Sci 1176: 55-69
55. Tokumura A, Majima E, Kariya Y, Tominaga K, Kogure K, Yasuda K, Fukuzawa K, (2002) Identification of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. J Biol Chem 277: 39436-39442
56. Umezu-Goto M, Kishi Y, Taira A, Hama K, Dohmae N, Takio K, Yamori T, Mills GB, Inoue K, Aoki J, Arai H, (2002) Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J Cell Biol 158: 227-233
57. Walmsley M, Cleaver D, Patient R, (2008) Fibroblast growth factor controls the timing of Scl, Lmo2, and Runx1 expression during embryonic blood development. Blood 111: 1157-1166
58. Warren AJ, Colledge WH, Carlton MB, Evans MJ, Smith AJ, Rabbitts TH, (1994) The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development. Cell 78: 45-57
59. Winnier G, Blessing M, Labosky PA, Hogan BL, (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105-2116
60. Yue R, Li H, Liu H, Li Y, Wei B, Gao G, Jin Y, Liu T, Wei L, Du J, Pei G, (2012) Thrombin receptor regulates hematopoiesis and endothelial-to- hematopoietic transition. Dev Cell 22: 1092-1100
61. Yukiura H, Hama K, Nakanaga K, Tanaka M, Asaoka Y, Okudaira S, Arima N, Inoue A, Hashimoto T, Arai H, Kawahara A, Nishina H, Aoki J, (2011) Autotaxin regulates vascular development via multiple lysophosphatidic acid (LPA) receptors in zebrafish. J Biol Chem 286: 43972-43983
62. Zafonte BT, Liu S, Lynch-Kattman M, Torregroza I, Benvenuto L, Kennedy M, Keller G, Evans T, (2007) Smad1 expands the hemangioblast population within a limited developmental window. Blood 109: 516-523
63. Zhang L, Magli A, Catanese J, Xu Z, Kyba M, Perlingeiro RC, (2011) Modulation of TGF-beta signaling by endoglin in murine hemangioblast development and primitive hematopoiesis. Blood 118: 88-97