Hemovascular progenitors in the kidney require sphingosine-1-phosphate receptor 1 for vascular development

Journal of the American Society of Nephrology

Volumn 27, Issue 7, 2016, Pages 1984-1995

  Hu, Yan ^a,b   Li, Minghong ^a   Göthert, Joachim R ^c   Gomez, R Ariel ^a   Sequeira Lopez, Maria Luisa S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CD31 ANTIGEN; DIPEPTIDYL CARBOXYPEPTIDASE; ERYTHROPOIETIN RECEPTOR; HEMOGLOBIN; HISTONE H3; MYOSIN HEAVY CHAIN; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 1; TAMOXIFEN; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG; S1PR1 PROTEIN, MOUSE;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL LINEAGE; CELL MATURATION; COLONY FORMING UNIT GEMM; COLONY FORMING UNIT GM; CONTROLLED STUDY; EMBRYO; ENDOTHELIAL PROGENITOR CELL; ERYTHROBLAST; GLOMERULUS CAPILLARY; HEMATOPOIETIC CELL; HISTONE PHOSPHORYLATION; IMMUNOHISTOCHEMISTRY; KIDNEY CAPSULE; KIDNEY DEVELOPMENT; KIDNEY MESENCHYME CELL; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; MESANGIUM CELL; MOUSE; NONHUMAN; PERICYTE; PRECURSOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM; ANIMAL; BLOOD VESSEL; EMBRYOLOGY; KIDNEY; ORGANOGENESIS; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; BLOOD VESSELS; ENDOTHELIUM, VASCULAR; KIDNEY; MICE; ORGANOGENESIS; RECEPTORS, LYSOSPHINGOLIPID;

EID: 85021848560     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015060610     Document Type: Article

References (50)

1. Sabin FR: Origin and development of the primitive vessels of the chick and of the pig. Contrib Embryol 6: 61–124, 1917
2. Lancrin C, Sroczynska P, Serrano AG, Gandillet A, Ferreras C, Kouskoff V, Lacaud G: Blood cell generation from the hemangioblast. J Mol Med (Berl) 88: 167–172, 2010
3. Liu F, Bhang SH, Arentson E, Sawada A, Kim CK, Kang I, Yu J, Sakurai N, Kim SH, Yoo JJ, Kim P, Pahng SH, Xia Y, Solnica-Krezel L, Choi K: Enhanced hemangioblast generation and improved vascular repair and regeneration from embryonic stem cells by defined transcription factors. Stem Cell Rep 1: 166–182, 2013
4. Kennedy M, Firpo M, Choi K, Wall C, Robertson S, Kabrun N, Keller G: A common precursor for primitive erythropoiesis and definitive haema-topoiesis. Nature 386: 488–493, 1997
5. Zambidis ET, Park TS, Yu W, Tam A, Levine M, Yuan X, Pryzhkova M, Péault B: Expression of angiotensin-converting enzyme (CD143) identifies and regulates primitive hemangioblasts derived from human pluripotent stem cells. Blood 112: 3601–3614, 2008
6. Tavian M, Biasch K, Sinka L, Vallet J, Péault B: Embryonic origin of human hematopoiesis. Int J Dev Biol 54: 1061–1065, 2010
7. Nishikawa S: Hemangioblast: An in vitro phantom. Wiley Interdiscip Rev Dev Biol 1: 603–608, 2012
8. Gering M, Rodaway AR, Göttgens B, Patient RK, Green AR: The SCL gene specifies haemangioblast development from early mesoderm. EMBO J 17: 4029–4045, 1998
9. Bloor AJ, Sánchez MJ, Green AR, Göttgens B: The role of the stem cell leukemia (SCL) gene in hematopoietic and endothelial lineage specification. J Hematother Stem Cell Res 11: 195–206, 2002
10. Göthert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, Green AR, Göttgens B, Izon DJ, Begley CG: Genetically tagging endothelial cells in vivo: Bone marrow-derived cells do not contribute to tumor endothelium. Blood 104: 1769–1777, 2004
11. Göthert JR, Gustin SE, Hall MA, Green AR, Göttgens B, Izon DJ, Begley CG: In vivo fate-tracing studies using the Scl stem cell enhancer: Embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood 105: 2724–2732, 2005
12. Sequeira Lopez ML, Pentz ES, Robert B, Abrahamson DR, Gomez RA: Embryonic origin and lineage of juxtaglomerular cells. Am J Physiol Renal Physiol 281: F345–F356, 2001
13. Sequeira Lopez ML, Chernavvsky DR, Nomasa T, Wall L, Yanagisawa M, Gomez RA: The embryo makes red blood cell progenitors in every tissue simultaneously with blood vessel morphogenesis. Am J Physiol Regul Integr Comp Physiol 284: R1126–R1137, 2003
14. Lin EE, Sequeira-Lopez ML, Gomez RA: RBP-J in FOXD1+ renal stromal progenitors is crucial for the proper development and assembly of the kidney vasculature and glomerular mesangial cells. Am J Physiol Renal Physiol 306: F249–F258, 2014
15. Sequeira-Lopez ML, Lin EE, Li M, Hu Y, Sigmund CD, Gomez RA: The earliest metanephric arteriolar progenitors and their role in kidney vascular development. Am J Physiol Regul Integr Comp Physiol 308: R138–R149, 2015
16. Kono M, Allende ML, Proia RL: Sphingosine-1-phosphate regulation of mammalian development. Biochim Biophys Acta 1781: 435–441, 2008
17. Kono M, Mi Y, Liu Y, Sasaki T, Allende ML, Wu YP, Yamashita T, Proia RL: The sphingosine-1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis. J Biol Chem 279: 29367–29373, 2004
18. Allende ML, Yamashita T, Proia RL: G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102: 3665–3667, 2003
19. 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: Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J Clin Invest 106: 951–961, 2000
20. de Bruijn MF, Speck NA, Peeters MC, Dzierzak E: Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 19: 2465–2474, 2000
21. Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, Yang Y, Becker MS, Zanetta L, Dejana E, Gasson JC, Tallquist MD, Iruela-Arispe ML: Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3: 625–636, 2008
22. Hasegawa T, McLeod DS, Bhutto IA, Prow T, Merges CA, Grebe R, Lutty GA: The embryonic human choriocapillaris develops by hemovasculogenesis. Dev Dyn 236: 2089–2100, 2007
23. Hyink DP, Tucker DC, St John PL, Leardkamolkarn V, Accavitti MA, Abrass CK, Abrahamson DR: Endogenous origin of glomerular endothelial and mesangial cells in grafts of embryonic kidneys. Am J Physiol 270: F886–F899, 1996
24. Loughna S, Hardman P, Landels E, Jussila L, Alitalo K, Woolf AS: A molecular and genetic analysis of renalglomerular capillary development. Angiogenesis 1: 84–101, 1997
25. Robert B, St John PL, Hyink DP, Abrahamson DR: Evidence that embryonic kidney cells expressing flk-1 are intrinsic, vasculogenic angio-blasts. Am J Physiol 271: F744–F753, 1996
26. Li Z, Lan Y, He W, Chen D, Wang J, Zhou F, Wang Y, Sun H, Chen X, Xu C, Li S, Pang Y, Zhang G, Yang L, Zhu L, Fan M, Shang A, Ju Z, Luo L, Ding Y, Guo W, Yuan W, Yang X, Liu B: Mouse embryonic head as a site for hematopoietic stem cell development. Cell Stem Cell 11: 663–675, 2012
27. Xiong Y, Yang P, Proia RL, Hla T: Erythrocyte-derived sphingosine 1-phosphate is essential for vascular development. J Clin Invest 124: 4823–4828, 2014
28. Ben Shoham A, Malkinson G, Krief S, Shwartz Y, Ely Y, Ferrara N, Yaniv K, Zelzer E: S1P1 inhibits sprouting angiogenesis during vascular development. Development 139: 3859–3869, 2012
29. 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, Adams R, Jakobsson L, Majumdar A, Vestweber D, Uv A, Betsholtz C: The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR2. Dev Cell 23: 587–599, 2012
30. Kikkawa Y, Virtanen I, Miner JH: Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin alpha5 in the glomerular basement membrane. J Cell Biol 161: 187–196, 2003
31. Lindahl P, Hellström M, Kalén M, Karlsson L, Pekny M, Pekna M, Soriano P, Betsholtz C: Paracrine PDGF-B/PDGF-Rbeta signaling controls mesangial cell development in kidney glomeruli. Development 125: 3313–3322, 1998
32. Vaughan MR, Quaggin SE: How do mesangial and endothelial cells form the glomerular tuft? J Am Soc Nephrol 19: 24–33, 2008
33. Takemoto M, He L, Norlin J, Patrakka J, Xiao Z, Petrova T, Bondjers C, Asp J, Wallgard E, Sun Y, Samuelsson T, Mostad P, Lundin S, Miura N, Sado Y, Alitalo K, Quaggin SE, Tryggvason K, Betsholtz C: Large-scale identification of genes implicated in kidney glomerulus development and function. EMBO J 25: 1160–1174, 2006
34. Quaggin SE, Schwartz L, Cui S, Igarashi P, Deimling J, Post M, Rossant J: The basic-helix-loop-helix protein pod1 is critically important for kidney and lung organogenesis. Development 126: 5771–5783, 1999
35. Dreyer SD, Zhou G, Baldini A, Winterpacht A, Zabel B, Cole W, Johnson RL, Lee B: Mutations in LMX1B cause abnormal skeletal patterning and renal dysplasia in nail patella syndrome. Nat Genet 19: 47–50, 1998
36. Chen H, Lun Y, Ovchinnikov D, Kokubo H, Oberg KC, Pepicelli CV, Gan L, Lee B, Johnson RL: Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat Genet 19: 51–55, 1998
37. Means CK, Brown JH: Sphingosine-1-phosphate receptor signalling in the heart. Cardiovasc Res 82: 193–200, 2009
38. Zhang J, Honbo N, Goetzl EJ, Chatterjee K, Karliner JS, Gray MO: Signals from type 1 sphingosine 1-phosphate receptors enhance adult mouse cardiac myocyte survival during hypoxia. Am J Physiol Heart Circ Physiol 293: H3150–H3158, 2007
39. Means CK, Xiao CY, Li Z, Zhang T, Omens JH, Ishii I, Chun J, Brown JH: Sphingosine 1-phosphate S1P2 and S1P3 receptor-mediated Akt activation protects against in vivo myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 292: H2944–H2951, 2007
40. Lee HW, Qin YX, Kim YM, Park EY, Hwang JS, Huo GH, Yang CW, Kim WY, Kim J: Expression of lymphatic endothelium-specific hyaluronan receptor LYVE-1 in the developing mouse kidney. Cell Tissue Res 343: 429–444, 2011
41. Srinivasan RS, Dillard ME, Lagutin OV, Lin FJ, Tsai S, Tsai MJ, Samokhvalov IM, Oliver G: Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 21: 2422–2432, 2007
42. Buttler K, Kreysing A, von Kaisenberg CS, Schweigerer L, Gale N, Papoutsi M, Wilting J: Mesenchymal cells with leukocyte and lym-phendothelial characteristics in murine embryos. Dev Dyn 235: 1554–1562, 2006
43. Sebzda E, Hibbard C, Sweeney S, Abtahian F, Bezman N, Clemens G, Maltzman JS, Cheng L, Liu F, Turner M, Tybulewicz V, Koretzky GA, Kahn ML: Syk and Slp-76 mutant mice reveal a cell-autonomous hematopoietic cell contribution to vascular development. Dev Cell 11: 349–361, 2006
44. Heinrich AC, Pelanda R, Klingmüller U: A mouse model for visualization and conditional mutations in the erythroid lineage. Blood 104: 659–666, 2004
45. Yu J, Carroll TJ, McMahon AP: Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 129: 5301–5312, 2002
46. Soriano P: Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70–71, 1999
47. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L: A global double-fluorescent Cre reporter mouse. Genesis 45: 593–605, 2007
48. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H: A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133–140, 2010
49. Wu S, Wu Y, Capecchi MR: Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development 133: 581–590, 2006
50. Sequeira López ML, Pentz ES, Nomasa T, Smithies O, Gomez RA: Renin cells are precursors for multiple cell types that switch to the renin phenotype when homeostasis is threatened. Dev Cell 6: 719–728, 2004