Gene expression programs of mouse endothelial cells in kidney development and disease

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Brunskill, Eric W ^a   Potter, S Steven ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS9 PROTEIN; ANGIOPOIETIN RECEPTOR; APELIN; APELIN RECEPTOR; BONE MORPHOGENETIC PROTEIN; CARRIER PROTEIN; CELL ADHESION MOLECULE; DECAY ACCELERATING FACTOR; ENDOTHELIAL SPECIFIC MOLECULE 1; FATTY ACID BINDING PROTEIN 7; GREEN FLUORESCENT PROTEIN; METALLOPROTEINASE; PHOSPHODIESTERASE; PROTEIN PDE7B; PROTEIN SERPINA3G; THROMBOMODULIN; TRANSFORMING GROWTH FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL DISRUPTION; CELL TYPE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; EMBRYO; ENDOTHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GLOMERULUS; KIDNEY CORTEX; KIDNEY DEVELOPMENT; KIDNEY DISEASE; KIDNEY MEDULLA; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EMBRYO; ANTIBODY SPECIFICITY; BLOOD VESSEL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; KIDNEY; METABOLISM; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; VASCULARIZATION;

MUS;

ANIMALS; BLOOD VESSELS; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; KIDNEY; KIDNEY DISEASES; MICE; MUTATION; ORGAN SPECIFICITY;

EID: 77957794382     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012034     Document Type: Article

References (93)

1. Stewart PA, Wiley MJ (1981) Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev Biol 84: 183-192.
2. Stainier DY, Fouquet B, Chen JN, Warren KS, Weinstein BM, et al. (1996) Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development 123: 285-292.
3. Lammert E, Cleaver O, Melton D (2001) Induction of pancreatic differentiation by signals from blood vessels. Science 294: 564-567.
4. Matsumoto K, Yoshitomi H, Rossant J, Zaret KS (2001) Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294: 559-563.
5. Abrahamson DR (2009) Development of kidney glomerular endothelial cells and their role in basement membrane assembly. Organogenesis 5: 275-287.
6. Cleaver O, Melton DA (2003) Endothelial signaling during development. Nat Med 9: 661-668.
7. Goligorsky MS, Chen J, Brodsky S (2001) Workshop: endothelial cell dysfunction leading to diabetic nephropathy: focus on nitric oxide. Hypertension 37: 744-748.
8. Yoon KH, Lee JH, Kim JW, Cho JH, Choi YH, et al. (2006) Epidemic obesity and type 2 diabetes in Asia. Lancet 368: 1681-1688.
9. Atkins RC, Zimmet P (2010) Diabetic kidney disease: act now or pay later. Nephrol Dial Transplant 25: 331-333.
10. Galkina E, Ley K (2006) Leukocyte recruitment and vascular injury in diabetic nephropathy. J Am Soc Nephrol 17: 368-377.
11. Zent R, Pozzi A (2007) Angiogenesis in diabetic nephropathy. Semin Nephrol 27: 161-171.
12. Isermann B, Vinnikov IA, Madhusudhan T, Herzog S, Kashif M, et al. (2007) Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat Med 13: 1349-1358.
13. Stuart RO, Bush KT, Nigam SK (2001) Changes in global gene expression patterns during development and maturation of the rat kidney. Proc Natl Acad Sci U S A 98: 5649-5654.
14. Challen G, Gardiner B, Caruana G, Kostoulias X, Martinez G, et al. (2005) Temporal and spatial transcriptional programs in murine kidney development. Physiol Genomics 23: 159-171.
15. Stuart RO, Bush KT, Nigam SK (2003) Changes in gene expression patterns in the ureteric bud and metanephric mesenchyme in models of kidney development. Kidney Int 64: 1997-2008.
16. Schwab K, Hartman HA, Liang HC, Aronow BJ, Patterson LT, et al. (2006) Comprehensive microarray analysis of Hoxa11/Hoxd11 mutant kidney development. Dev Biol 293: 540-554.
17. Brunskill EW, Aronow BJ, Georgas K, Rumballe B, Valerius MT, et al. (2008) Atlas of gene expression in the developing kidney at microanatomic resolution. Dev Cell 15: 781-791.
18. De Val S, Black BL (2009) Transcriptional control of endothelial cell development. Dev Cell 16: 180-195.
19. Goldie LC, Nix MK, Hirschi KK (2008) Embryonic vasculogenesis and hematopoietic specification. Organogenesis 4: 257-263.
20. Guo Y, Chan R, Ramsey H, Li W, Xie X, et al. (2003) The homeoprotein Hex is required for hemangioblast differentiation. Blood 102: 2428-2435.
21. Broxmeyer HE, Sehra S, Cooper S, Toney LM, Kusam S, et al. (2007) Aberrant regulation of hematopoiesis by T cells in BAZF-deficient mice. Mol Cell Biol 27: 5275-5285.
22. Lacorazza HD, Yamada T, Liu Y, Miyata Y, Sivina M, et al. (2006) The transcription factor MEF/ELF4 regulates the quiescence of primitive hematopoietic cells. Cancer Cell 9: 175-187.
23. Sequeira Lopez ML, Chernavvsky DR, Nomasa T, Wall L, Yanagisawa M, et al. (2003) The embryo makes red blood cell progenitors in every tissue simultaneously with blood vessel morphogenesis. Am J Physiol Regul Integr Comp Physiol 284: R1126-1137.
24. Sumanas S, Lin S (2006) Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol 4: e10.
25. Valdembri D, Serini G, Vacca A, Ribatti D, Bussolino F (2002) In vivo activation of JAK2/STAT-3 pathway during angiogenesis induced by GM-CSF. FASEB J 16: 225-227.
26. Niu G, Wright KL, Huang M, Song L, Haura E, et al. (2002) Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 21: 2000-2008.
27. Emerson GG, Segal SS (2001) Electrical activation of endothelium evokes vasodilation and hyperpolarization along hamster feed arteries. Am J Physiol Heart Circ Physiol 280: H160-167.
28. Bossu JL, Elhamdani A, Feltz A (1992) Voltage-dependent calcium entry in confluent bovine capillary endothelial cells. FEBS Lett 299: 239-242.
29. Naslavsky N, McKenzie J, Altan-Bonnet N, Sheff D, Caplan S (2009) EHD3 regulates early-endosome-to-Golgi transport and preserves Golgi morphology. J Cell Sci 122: 389-400.
30. Patrakka J, Xiao Z, Nukui M, Takemoto M, He L, et al. (2007) Expression and subcellular distribution of novel glomerulus-associated proteins dendrin, ehd3, sh2d4a, plekhh2, and 2310066E14Rik. J Am Soc Nephrol 18: 689-697.
31. Nemer G, Nemer M (2002) Cooperative interaction between GATA5 and NF-ATc regulates endothelial-endocardial differentiation of cardiogenic cells. Development 129: 4045-4055.
32. Sadanandam A, Rosenbaugh EG, Singh S, Varney M, Semaphorin SinghRK (2009) 5A promotes angiogenesis by increasing endothelial cell proliferation, migration, and decreasing apoptosis. Microvasc Res 79: 1-9.
33. McCulloch DR, Le Goff C, Bhatt S, Dixon LJ, Sandy JD, et al. (2009) Adamts5, the gene encoding a proteoglycan-degrading metalloprotease, is expressed by specific cell lineages during mouse embryonic development and in adult tissues. Gene Expr Patterns 9: 314-323.
34. Sharghi-Namini S, Fan H, Sulochana KN, Potturi P, Xiang W, et al. (2008) The first but not the second thrombospondin type 1 repeat of ADAMTS5 functions as an angiogenesis inhibitor. Biochem Biophys Res Commun 371: 215-219.
35. Krucken J, Schroetel RM, Muller IU, Saidani N, Marinovski P, et al. (2004) Comparative analysis of the human gimap gene cluster encoding a novel GTPase family. Gene 341: 291-304.
36. Satchell SC, Braet F (2009) Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol Renal Physiol 296: F947-956.
37. Neuhofer W, Beck FX (2005) Cell survival in the hostile environment of the renal medulla. Annu Rev Physiol 67: 531-555.
38. Kondo T, Vicent D, Suzuma K, Yanagisawa M, King GL, et al. (2003) Knockout of insulin and IGF-1 receptors on vascular endothelial cells protects against retinal neovascularization. J Clin Invest 111: 1835-1842.
39. Shigematsu S, Yamauchi K, Nakajima K, Iijima S, Aizawa T, et al. (1999) IGF-1 regulates migration and angiogenesis of human endothelial cells. Endocr J. 46. pp. S59-62.
40. Fukuda R, Hirota K, Fan F, Jung YD, Ellis LM, et al. (2002) Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J Biol Chem 277: 38205-38211.
41. Clark TG, Conway SJ, Scott IC, Labosky PA, Winnier G, et al. (1999) The mammalian Tolloid-like 1 gene, Tll1, is necessary for normal septation and positioning of the heart. Development 126: 2631-2642.
42. Stojic J, Hagemann C, Haas S, Herbold C, Kuhnel S, et al. (2008) Expression of matrix metalloproteinases MMP-1, MMP-11 and MMP-19 is correlated with the WHO-grading of human malignant gliomas. Neurosci Res 60: 40-49.
43. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, et al. (1997) Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55-60.
44. Breyer MD, Bottinger E, Brosius FC 3rd, Coffman TM, Harris RC, et al. (2005) Mouse models of diabetic nephropathy. J Am Soc Nephrol 16: 27-45.
45. Cohen MP, Clements RS, Hud E, Cohen JA, Ziyadeh FN (1996) Evolution of renal function abnormalities in the db/db mouse that parallels the development of human diabetic nephropathy. Exp Nephrol 4: 166-171.
46. Furuta T, Saito T, Ootaka T, Soma J, Obara K, et al. (1993) The role of macrophages in diabetic glomerulosclerosis. Am J Kidney Dis 21: 480-485.
47. Sassy-Prigent C, Heudes D, Mandet C, Belair MF, Michel O, et al. (2000) Early glomerular macrophage recruitment in streptozotocin-induced diabetic rats. Diabetes 49: 466-475.
48. Chow F, Ozols E, Nikolic-Paterson DJ, Atkins RC, Tesch GH (2004) Macrophages in mouse type 2 diabetic nephropathy: correlation with diabetic state and progressive renal injury. Kidney Int 65: 116-128.
49. Okada S, Shikata K, Matsuda M, Ogawa D, Usui H, et al. (2003) Intercellular adhesion molecule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes 52: 2586-2593.
50. Chow FY, Nikolic-Paterson DJ, Ozols E, Atkins RC, Tesch GH (2005) Intercellular adhesion molecule-1 deficiency is protective against nephropathy in type 2 diabetic db/db mice. J Am Soc Nephrol 16: 1711-1722.
51. Hirata K, Shikata K, Matsuda M, Akiyama K, Sugimoto H, et al. (1998) Increased expression of selectins in kidneys of patients with diabetic nephropathy. Diabetologia 41: 185-192.
52. Pall AA, Garner CM, Richards GM, Howie AJ, Adu D, et al. (1993) Expression of E-selectin in the human kidney. Nephrol Dial Transplant 8: 1429-1430.
53. Shankland SJ (2006) The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int 69: 2131-2147.
54. Nguyen TQ, Roestenberg P, van Nieuwenhoven FA, Bovenschen N, Li Z, et al. (2008) CTGF inhibits BMP-7 signaling in diabetic nephropathy. J Am Soc Nephrol 19: 2098-2107.
55. Wang S, Chen Q, Simon TC, Strebeck F, Chaudhary L, et al. (2003) Bone morphogenic protein-7 (BMP-7), a novel therapy for diabetic nephropathy. Kidney Int 63: 2037-2049.
56. Sugimoto H, Grahovac G, Zeisberg M, Kalluri R (2007) Renal fibrosis and glomerulosclerosis in a new mouse model of diabetic nephropathy and its regression by bone morphogenic protein-7 and advanced glycation end product inhibitors. Diabetes 56: 1825-1833.
57. Wang S, de Caestecker M, Kopp J, Mitu G, Lapage J, et al. (2006) Renal bone morphogenetic protein-7 protects against diabetic nephropathy. J Am Soc Nephrol 17: 2504-2512.
58. Moser M, Binder O, Wu Y, Aitsebaomo J, Ren R, et al. (2003) BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol Cell Biol 23: 5664-5679.
59. Ikeya M, Kawada M, Kiyonari H, Sasai N, Nakao K, et al. (2006) Essential pro-Bmp roles of crossveinless 2 in mouse organogenesis. Development 133: 4463-4473.
60. Chen S, Jim B, Ziyadeh FN (2003) Diabetic nephropathy and transforming growth factor-beta: transforming our view of glomerulosclerosis and fibrosis build-up. Semin Nephrol 23: 532-543.
61. Sharma K, Jin Y, Guo J, Ziyadeh FN (1996) Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 45: 522-530.
62. Ziyadeh FN, Hoffman BB, Han DC, Iglesias-De La, Cruz MC, Hong SW, et al. (2000) Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc Natl Acad Sci U S A 97: 8015-8020.
63. Ishida J, Hashimoto T, Hashimoto Y, Nishiwaki S, Iguchi T, et al. (2004) Regulatory roles for APJ, a seven-transmembrane receptor related to angiotensin-type 1 receptor in blood pressure in vivo. J Biol Chem 279: 26274-26279.
64. Kleinz MJ, Skepper JN, Davenport AP (2005) Immunocytochemical localisation of the apelin receptor, APJ, to human cardiomyocytes, vascular smooth muscle and endothelial cells. Regul Pept 126: 233-240.
65. Hus-Citharel A, Bouby N, Frugiere A, Bodineau L, Gasc JM, et al. (2008) Effect of apelin on glomerular hemodynamic function in the rat kidney. Kidney Int 74: 486-494.
66. Zhong JC, Huang Y, Yung LM, Lau CW, Leung FP, et al. (2007) The novel peptide apelin regulates intrarenal artery tone in diabetic mice. Regul Pept 144: 109-114.
67. Zhong JC, Yu XY, Huang Y, Yung LM, Lau CW, et al. (2007) Apelin modulates aortic vascular tone via endothelial nitric oxide synthase phosphorylation pathway in diabetic mice. Cardiovasc Res 74: 388-395.
68. Kalin RE, Kretz MP, Meyer AM, Kispert A, Heppner FL, et al. (2007) Paracrine and autocrine mechanisms of apelin signaling govern embryonic and tumor angiogenesis. Dev Biol 305: 599-614.
69. Kleinz MJ, Davenport AP (2005) Emerging roles of apelin in biology and medicine. Pharmacol Ther 107: 198-211.
70. Tatemoto K, Takayama K, Zou MX, Kumaki I, Zhang W, et al. (2001) The novel peptide apelin lowers blood pressure via a nitric oxide-dependent mechanism. Regul Pept 99: 87-92.
71. Jia YX, Lu ZF, Zhang J, Pan CS, Yang JH, et al. (2007) Apelin activates L-arginine/nitric oxide synthase/nitric oxide pathway in rat aortas. Peptides 28: 2023-2029.
72. Prabhakar SS (2004) Role of nitric oxide in diabetic nephropathy. Semin Nephrol 24: 333-344.
73. Lassalle P, Molet S, Janin A, Heyden JV, Tavernier J, et al. (1996) ESM-1 is a novel human endothelial cell-specific molecule expressed in lung and regulated by cytokines. J Biol Chem 271: 20458-20464.
74. van Lunteren E, Moyer M (2009) Gene expression profiling in the type 1 diabetes rat diaphragm. PLoS One 4: e7832.
75. Shin JW, Huggenberger R, Detmar M (2008) Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis. Blood 112: 2318-2326.
76. Bechard D, Scherpereel A, Hammad H, Gentina T, Tsicopoulos A, et al. (2001) Human endothelial-cell specific molecule-1 binds directly to the integrin CD11a/CD18 (LFA-1) and blocks binding to intercellular adhesion molecule-1. J Immunol 167: 3099-3106.
77. Demircan K, Hirohata S, Nishida K, Hatipoglu OF, Oohashi T, et al. (2005) ADAMTS-9 is synergistically induced by interleukin-1beta and tumor necrosis factor alpha in OUMS-27 chondrosarcoma cells and in human chondrocytes. Arthritis Rheum 52: 1451-1460.
78. Koo BH, Coe DM, Dixon LJ, Somerville RP, Nelson CM, et al. ADAMTS9 is a cell-autonomously acting, anti-angiogenic metalloprotease expressed by microvascular endothelial cells. Am J Pathol 1494-1504.
79. Skubitz KM, Zimmermann W, Kammerer R, Pambuccian S, Skubitz AP (2006) Differential gene expression identifies subgroups of renal cell carcinoma. J Lab Clin Med 147: 250-267.
80. Beigneux AP, Davies BS, Gin P, Weinstein MM, Farber E, et al. (2007) Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab 5: 279-291.
81. Liu N, Wang Y, Ashton-Rickardt PG (2004) Serine protease inhibitor 2A inhibits caspase-independent cell death. FEBS Lett 569: 49-53.
82. He P, Zeng M, Curry FE (2000) Dominant role of cAMP in regulation of microvessel permeability. Am J Physiol Heart Circ Physiol 278: H1124-1133.
83. Waschke J, Drenckhahn D, Adamson RH, Barth H, Curry FE (2004) cAMP protects endothelial barrier functions by preventing Rac-1 inhibition. Am J Physiol Heart Circ Physiol 287: H2427-2433.
84. Min W, Yamanaka N (1993) Three-dimensional analysis of increased vasculature around the glomerular vascular pole in diabetic nephropathy. Virchows Arch A Pathol Anat Histopathol 423: 201-207.
85. Osterby R, Asplund J, Bangstad HJ, Nyberg G, Rudberg S, et al. (1999) Neovascularization at the vascular pole region in diabetic glomerulopathy. Nephrol Dial Transplant 14: 348-352.
86. Osterby R, Nyberg G (1987) New vessel formation in the renal corpuscles in advanced diabetic glomerulopathy. J Diabet Complications 1: 122-127.
87. Stout LC, Whorton EB (2007) Pathogenesis of extra efferent vessel development in diabetic glomeruli. Hum Pathol 38: 1167-1177.
88. Kato H, Si H, Hostetter T, Susztak K (2008) Smad1 as a biomarker for diabetic nephropathy. Diabetes 57: 1459-1460.
89. Susztak K, Bottinger E, Novetsky A, Liang D, Zhu Y, et al. (2004) Molecular profiling of diabetic mouse kidney reveals novel genes linked to glomerular disease. Diabetes 53: 784-794.
90. Wada J, Zhang H, Tsuchiyama Y, Hiragushi K, Hida K, et al. (2001) Gene expression profile in streptozotocin-induced diabetic mice kidneys undergoing glomerulosclerosis. Kidney Int 59: 1363-1373.
91. Knoll KE, Pietrusz JL, Liang M (2005) Tissue-specific transcriptome responses in rats with early streptozotocin-induced diabetes. Physiol Genomics 21: 222-229.
92. Wu Y, Liu Z, Xiang Z, Zeng C, Chen Z, et al. (2006) Obesity-related glomerulopathy: insights from gene expression profiles of the glomeruli derived from renal biopsy samples. Endocrinology 147: 44-50.
93. Baelde HJ, Eikmans M, Doran PP, Lappin DW, de Heer E, et al. (2004) Gene expression profiling in glomeruli from human kidneys with diabetic nephropathy. Am J Kidney Dis 43: 636-650.