Postnatal development of the renal medulla; role of the renin-angiotensin system

Acta Physiologica

Volumn 208, Issue 1, 2013, Pages 41-49

  Madsen, K ^a,b   Tinning, A R ^b   Marcussen, N ^a   Jensen, B L ^b  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Development; Hypertension; Renal medulla; Renin angiotensin system

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; AQUAPORIN 2; MESSENGER RNA; RENIN; VASCULOTROPIN;

ALLELE; ANGIOGENESIS; BLOOD PRESSURE REGULATION; CELL PROLIFERATION; CELL SURVIVAL; ENDOTHELIUM CELL; FETUS DEVELOPMENT; HEMANGIOBLAST; HUMAN; HYPERTENSION; KIDNEY BLOOD FLOW; KIDNEY BLOOD VESSEL; KIDNEY DEVELOPMENT; KIDNEY MEDULLA; MAMMAL; MATURITY; MICROCIRCULATION; NEPHRON; NONHUMAN; PATHOPHYSIOLOGY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION;

AGE FACTORS; ANGIOGENIC PROTEINS; ANIMALS; HEMODYNAMICS; HUMANS; HYPERTENSION; KIDNEY MEDULLA; MICROCIRCULATION; PROGNOSIS; RENAL CIRCULATION; RENIN-ANGIOTENSIN SYSTEM; RISK FACTORS; SIGNAL TRANSDUCTION; UROGENITAL ABNORMALITIES;

EID: 84876332141     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12088     Document Type: Review

References (96)

1. 1 receptor mRNA in rat kidney. Kidney Int 46, 973-979.
2. Barker, D.J., Osmond, C., Golding, J., Kuh, D. & Wadsworth, M.E. 1989. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298, 564-567.
3. Berger, S., Bleich, M., Schmid, W., Cole, T.J., Peters, J., Watanabe, H., Kriz, W., Warth, R., Greger, R. & Schütz, G. 1998. Mineralocorticoid receptor knockout mice: pathophysiology of Na+ metabolism. Proc Natl Acad Sci USA 95, 9424-9429.
4. Bleich, M., Warth, R., Schmidt-Hieber, M., Schulz-Baldes, A., Hasselblatt, P., Fisch, D., Berger, S., Kunzelmann, K., Kriz, W., Schütz, G. & Greger, R. 1999. Rescue of the mineralocorticoid receptor knock-out mouse. Pflügers Arch 438, 245-254.
5. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C. et al. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439.
6. Celsi, G., Kistner, A., Aizman, R., Eklöf, A.C., Ceccatelli, S., de Santiago, A. & Jacobson, S.H. 1998. Prenatal dexamethasone causes oligonephronia, sodium retention and higher blood pressure in the offspring. Pediatr Res 44, 317-322.
7. Cha, J.H., Kim, Y.H., Jung, J.Y., Han, K.H., Madsen, K.M. & Kim, J. 2001. Cell proliferation in the loop of Henle in the developing rat kidney. J Am Soc Nephrol 12, 1410-1421.
8. Chen, X., Li, W., Yoshida, H., Tsuchida, S., Nishimura, H., Takemoto, F., Okubo, S., Fogo, A., Matsusaka, T. & Ichikawa, I. 1997. Targeting deletion of angiotensin type 1B receptor gene in the mouse. Am J Physiol 272, F299-F304.
9. Costerousse, O., Allegrini, J., Huang, H., Bounhik, J. & Alhenc-Gelas, F. 1994. Regulation of ACE gene expression and plasma levels during rat postnatal development. Am J Physiol 267, E745-E753.
10. Cruciat, C.M., Ohkawara, B., Acebron, S.P., Karaulanov, E., Reinhard, C., Ingelfinger, D., Boutros, M. & Niehrs, C. 2010. Requirement of prorenin receptor and vacuolar H + -ATPase-mediated acidification for Wnt signaling. Science 327, 459-463.
11. Daïkha-Dahmane, F., Levy-Beff, E., Jugie, M. & Lenclen, R. 2006. Foetal kidney maldevelopment in maternal use of angiotensin II type I receptor antagonists. Pediatr Nephrol 21, 729-732.
12. Dumont, D.J., Gradwohl, G., Fong, G.H., Puri, M.C., Gertsenstein, M., Auerbach, A. & Breitman, M.L. 1994. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev 8, 1897-1909.
13. Dymsza, H.A., Czajka, D.M. & Miller, S.A. 1964. Influence of artificial diet on weight gain and body composition of the neonatal rat. J Nutr 84, 100-106.
14. Eremina, V., Sood, M., Haigh, J., Nagy, A., Lajoie, G., Ferrara, N., Gerber, H.P., Kikkawa, Y., Miner, J.H. & Quaggin, S.E. 2003. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111, 707-716.
15. Feliers, D., Duraisamy, S., Barnes, J.L., Ghosh-Choudhury, G. & Kasinath, B.S. 2005. Translational regulation of vascular endothelial growth factor expression in renal epithelial cells by angiotensin II. Am J Physiol Renal Physiol 288, F521-F529.
16. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O′Shea, K.S., Powell-Braxton, L., Hillan, K.J. & Moore, M.W. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442.
17. Fong, G.H., Rossant, J., Gertsenstein, M. & Breitman, M.L. 2002. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376, 66-70.
18. Friberg, P., Sundelin, B., Bohman, S.O., Bobik, A., Nilsson, H., Wickman, A., Gustafsson, H., Petersen, J. & Adams, M.A. 1994. Renin-angiotensin system in neonatal rats: induction of a renal abnormality in response to ACE inhibition or angiotensin II antagonism. Kidney Int 45, 485-492.
19. Gale, N.W., Thurston, G., Hackett, S.F., Renard, R., Wang, Q., McClain, J., Martin, C., Witte, C., Witte, M.H., Jackson, D., Suri, C., Campochiaro, P.A., Wiegand, S.J. & Yancopoulos, G.D. 2002. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by angiopoietin-1. Dev Cell 3, 411-423.
20. Gerber, H.P., Hillan, K.J., Ryan, A.M., Kowalski, J., Keller, G.A., Rangell, L., Wright, B.D., Radtke, F., Aguet, M. & Ferrara, N. 1999. VEGF is required for growth and survival in neonatal mice. Development 126, 1149-1159.
21. Gomez, R.A., Lynch, K.R., Sturgill, B.C., Elwood, J.P., Chevalier, R.L., Carey, R.M. & Peach, M.J. 1989. Distribution of renin mRNA and its protein in the developing kidney. Am J Physiol 257, F850-F858.
22. Gomez, R.A., Norwood, V.F. & Tufro-McReddie, A. 1997. Development of the kidney vasculature. Microsc Res Tech 39, 254-260.
23. Guron, G., Adams, M.A., Sundelin, B. & Friberg, P. 1997. Neonatal angiotensin-converting enzyme inhibition in the rat induces persistent abnormalities in renal function and histology. Hypertension 29, 91-97.
24. Guron, G., Marcussen, N., Nilsson, A., Sundelin, B. & Friberg, P. 1999a. Postnatal time frame for renal vulnerability to enalapril in rats. J Am Soc Nephrol 10, 1550-1560.
25. Guron, G., Nilsson, A., Nitescu, N., Nielsen, S., Sundelin, B., Frøkiær, J. & Friberg, P. 1999b. Mechanisms of impaired urinary concentrating ability in adult rats treated neonatally with enalapril. Acta Physiol Scand 165, 103-112.
26. Hein, L., Barsh, G.S., Pratt, R.E., Dzau, V.J. & Kobilka, B.K. 1995. Behavioural and cardiovascular effects of disrupting the angiotensin II type-2 receptor gene in mice. Nature 377, 744-747.
27. Hilgers, K.F., Reddi, V., Krege, J.H., Smithies, O. & Gomez, R.A. 1997. Aberrant renal vascular morphology and renin expression in mutant mice lacking angiotensin-converting enzyme. Hypertension 29, 216-221.
28. Ichihara, A., Kaneshiro, Y., Takemitsu, T., Sakoda, M. & Itoh, H. 2007. The (pro)renin receptor and the kidney. Semin Nephrol 27, 524-528.
29. Jeansson, M., Gawlik, A., Anderson, G., Li, C., Kerjaschki, D., Henkelman, M. & Quaggin, S.E. 2011. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest 121, 2278-2289.
30. Jose, P.A., Logan, A.G., Slotkoff, L.M., Lilienfield, L.S., Calcagno, P.L. & Eisner, G.M. 1971. Intrarenal blood flow distribution in canine puppies. Pediatr Res 5, 335-344.
31. Keller, G., Zimmer, G., Mall, G., Ritz, E. & Amann, K. 2003. Nephron number in patients with primary hypertension. N Engl J Med 348, 101-108.
32. Kim, J., Lee, G.S., Tisher, C.C. & Madsen, K.M. 1996. Role of apoptosis in development of the ascending thin limb of the loop of Henle in rat kidney. Am J Physiol 271, F831-F845.
33. Kim, J., Kim, W.Y., Han, K.H., Knepper, M.A., Nielsen, S. & Madsen, K.M. 1999. Developmental expression of aquaporin-1 in the rat renal vasculature. Am J Physiol 276, F498-F509.
34. Kim, Y.H., Kim, D.U., Han, K.H., Jung, J.Y., Sands, J.M., Knepper, M.A., Madsen, K.M. & Kim, J. 2002. Expression of urea transporters in the developing rat kidney. Am J Physiol Renal Physiol 282, F530-F540.
35. Kitamoto, Y., Tokunaga, H. & Tomita, K. 1997. Vascular endothelial growth factor is an essential molecule for mouse kidney development: glomerulogenesis and nephrogenesis. J Clin Invest 99, 2351-2357.
36. Lee, G., Makhanova, N., Caron, K., Sequeira Lopez, M.L., Gomez, R.A., Smithies, O. & Kim, H.S. 2005. Homeostatic responses in the adrenal cortex to the absence of aldosterone in mice. Endocrinology 146, 2650-2656.
37. Leung, D.W., Cachianes, G., Kuang, W.J., Goeddel, D.V. & Ferrara, N. 1989. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246, 1306-1309.
38. Lochard, N., Silversides, D.W., van Kats, J.P., Mercure, C. & Reudelhuber, T.L. 2003. Brain-specific restoration of angiotensin II corrects renal defects seen in angiotensinogen-deficient mice. J Biol Chem 278, 2184-2189.
39. Loria, A., Reverte, V., Salazar, F., Saez, F., Llinas, M.T. & Salazar, F.J. 2007. Sex and age differences of renal function in rats with reduced ANG II activity during the nephrogenic period. Am J Physiol Renal Physiol 293, F506-F510.
40. Lu, S.H., Mattson, D.L. & Cowley, A.W. Jr. 1994. Renal medullary captopril delivery lowers blood pressure in spontaneously hypertensive rats. Hypertension 23, 337-345.
41. Madsen, K., Stubbe, J., Yang, T., Skøtt, O., Bachmann, S. & Jensen, B.L. 2004. Low endogenous glucocorticoid allows induction of kidney cortical cyclooxygenase-2 during postnatal rat development. Am J Physiol Renal Physiol 286, F26-F37.
42. Madsen, K., Marcussen, N., Pedersen, M., Kjaersgaard, G., Facemire, C., Coffman, T.M. & Jensen, B.L. 2010. Angiotensin II promotes development of the renal microcirculation through AT1 receptors. J Am Soc Nephrol 21, 448-459.
43. Makhanova, N., Lee, G., Takahashi, N., Sequeira Lopez, M.L., Gomez, R.A., Kim, H.S. & Smithies, O. 2006. Kidney function in mice lacking aldosterone. Am J Physiol Renal Physiol 290, F61-F69.
44. Mattot, V., Moons, L., Lupu, F., Chernavvsky, D., Gómez, R.A., Collen, D. & Carmeliet, P. 2002. Loss of the VEGF(164) and VEGF(188) isoforms impairs postnatal glomerular angiogenesis and renal arteriogenesis in mice. J Am Soc Nephrol 13, 1548-1560.
45. McCausland, J.E., Bertram, J.F., Ryan, G.B. & Alcorn, D. 1997. Glomerular number and size following chronic angiotensin II blockade in the postnatal rat. Exp Nephrol 5, 201-209.
46. Miyazaki, Y., Tsuchida, S., Nishimura, H., Pope, J.C. 4th, Harris, R.C., McKanna, J.M., Inagami, T., Hogan, B.L.M., Fogo, A. & Ichikawa, I. 1998. Angiotensin induces the urinary peristaltic machinery during the postnatal period. J Clin Invest 102, 1489-1497.
47. Miyazaki, Y., Tsuchida, S., Fogo, A. & Ichikawa, I. 1999. The renal lesions that develop in neonatal mice during angiotensin inhibition mimic obstructive nephropathy. Kidney Int 55, 1683-1695.
48. Nagata, M., Tanimoto, K., Fukamizu, A., Kon, Y., Sugiyama, F., Yagami, K., Murakami, K. & Watanabe, T. 1996. Nephrogenesis and renovascular development in angiotensinogen-deficient mice. Lab Invest 75, 745-753.
49. Neubauer, B., Machura, K., Chen, M., Weinstein, L.S., Oppermann, M., Sequeira Lopez, M.L., Gomez, R.A., Schnermann, J., Castrop, H., Kurtz, A. & Wagner, C. 2009. Development of vascular renin expression in the kidney critically depends on the cyclic AMP pathway. Am J Physiol Renal Physiol 296, F1006-F1012.
50. Norwood, V.F., Craig, M.R., Harris, J.M. & Gomez, R.A. 1997. Differential expression of angiotensin II receptors during early renal morphogenesis. Am J Physiol 272, R662-R668.
51. Oliverio, M.I., Kim, H.S., Ito, M., Le, T., Audoly, L., Best, C.F., Hiller, S., Kluckman, K., Maeda, N., Smithies, O. & Coffman, T.M. 1998a. Reduced growth, abnormal kidney structure, and type 2 (AT2) angiotensin receptor-mediated blood pressure regulation in mice lacking both AT1A and AT1B receptors for angiotensin II. Proc Natl Acad Sci USA 95, 15496-15501.
52. Oliverio, M.I., Madsen, K., Best, C.F., Ito, M., Maeda, N., Smithies, O. & Coffman, T.M. 1998b. Renal growth and development in mice lacking AT1A receptors for angiotensin II. Am J Physiol 274, F43-F50.
53. Ortiz, L.A., Quan, A., Weinberg, A. & Baum, M. 2001. Effect of prenatal dexamethasone on rat renal development. Kidney Int 59, 1663-1669.
54. Oshima, Y., Kinouchi, K., Ichihara, A., Sakoda, M., Kurauchi-Mito, A., Bokuda, K., Narita, T., Kurosawa, H., Sun-Wada, G.H., Wada, Y., Yamada, T., Takemoto, M., Saleem, M.A., Quaggin, S.E. & Itho, H. 2011. Prorenin receptor is essential for normal podocyte structure and function. J Am Soc Nephrol 22, 2203-2212.
55. Pannabecker, T.L. & Dantzler, W.H. 2006. Three-dimensional architecture of inner medullary vasa recta. Am J Physiol Renal Physiol 290, F1355-F1366.
56. Pitera, J.E., Woolf, A.S., Gale, N.W., Yancopoulos, G.D. & Yuan, H.T. 2004. Dysmorphogenesis of kidney cortical peritubular capillaries in angiopoietin-2-deficient mice. Am J Pathol 165, 1895-1906.
57. Polacek, E., Vocel, J., Neugebauerova, L., Sebkova, M. & Vechetova, E. 1965. The osmotic concentrating ability in healthy infants and children. Arch Dis Child 40, 291-295.
58. Rane, S. & Aperia, A. 1985. Ontogeny of Na-K-ATPase activity in thick ascending limb and of concentrating capacity. Am J Physiol 249, F723-F728.
59. Rane, S., Aperia, A., Eneroth, P. & Lundin, S. 1985. Development of urinary concentrating capacity in weaning rats. Pediatr Res 19, 472-475.
60. Reddi, V., Zaglul, A., Pentz, E.S. & Gomez, R.A. 1998. Renin-expressing cells are associated with branching of the developing kidney vasculature. J Am Soc Nephrol 9, 63-71.
61. Rizkalla, B., Forbes, J.M., Cooper, M.E. & Cao, Z. 2003. Increased renal vascular endothelial growth factor and angiopoietins by angiotensin II infusion is mediated by both AT1 and AT2 receptors. J Am Soc Nephrol 14, 3061-3071.
62. Robert, B., St John, P.L., Hyink, D.P. & Abrahamson, D.R. 1996. Evidence that embryonic kidney cells expressing flk-1 are intrinsic, vasculogenic angioblasts. Am J Physiol 271, F744-F753.
63. Robillard, J.E., Weismann, D.N. & Herin, P. 1981. Ontogeny of single glomerular perfusion rate in fetal and newborn lambs. Pediatr Res 15, 1248-1255.
64. Roman, R.J. & Kaldunski, M.L. 1988. Renal cortical and papillary blood flow in spontaneously hypertensive rats. Hypertension 11, 657-663.
65. Saez, F., Castells, M.T., Zuasti, A., Salazar, F., Reverte, V., Loria, A. & Salazar, F.J. 2007. Sex differences in the renal changes elicited by angiotensin II blockade during the nephrogenic period. Hypertension 49, 1429-1435.
66. Salazar, F., Reverte, V., Saez, F., Loria, A., Llinas, M.T. & Salazar, F.J. 2008. Age- and sodium-sensitive hypertension and sex-dependent renal changes in rats with a reduced nephron number. Hypertension 51, 1184-1189.
67. Sariola, H., Ekblom, P., Lehtonen, E. & Saxén, L. 1983. Differentiation and vascularization of the metanephric kidney grafted on the chorioallantoic membrane. Dev Biol 96, 427-435.
68. Sauter, A., Machura, K., Neubauer, B., Kurtz, A. & Wagner, C. 2008. Development of renin expression in the mouse kidney. Kidney Int 73, 43-51.
69. Senger, D.R., Galli, S.J., Dvorak, A.M., Perruzzi, C.A., Harvey, V.S. & Dvorak, H.F. 1983. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219, 983-985.
70. Sequeira Lopez, M.L. & Gomez, R.A. 2011. Development of the renal arterioles. J Am Soc Nephrol 22, 2156-2165.
71. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, W.F., Breitman, M.L. & Schuh, A.C. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-66.
72. Shanmugam, S., Corvol, P. & Gasc, J.M. 1994. Ontogeny of the two angiotensin II type 1 receptor subtypes in rats. Am J Physiol 267, E828-E836.
73. Shanmugam, S., Llorens-Cortes, C., Clauser, E., Corvol, P. & Gasc, J.M. 1995. Expression of angiotensin II AT2 receptor mRNA during development of rat kidney and adrenal gland. Am J Physiol 268, F922-F930.
74. Simon, M., Gröne, H.J., Jöhren, O., Kullmer, J., Plate, K.H., Risau, W. & Fuchs, E. 1995. Expression of vascular endothelial growth factor and its receptors in human renal ontogenesis and in adult kidney. Am J Physiol 268, F240-F250.
75. Song, R. & Yosypiv, I.V. 2012. Development of the kidney medulla. Organogenesis 8, 10-17.
76. Song, R., Preston, G. & Yosypiv, I.V. 2011. Angiotensin II stimulates in vitro branching morphogenesis of the isolated ureteric bud. Mech Dev 128, 359-367.
77. Song, R., Preston, G., Khalili, A., El-Dahr, S.S. & Yosypiv, I.V. 2012. Angiotensin II regulates growth of the developing papillas ex vivo. Am J Physiol Renal Physiol 302, F1112-F1120.
78. Speller, A.M. & Moffat, D.B. 1977. Tubulo-vascular relationships in developing kidney. J Anat 123, 487-500.
79. Stubbe, J., Jensen, B.L., Bachmann, S., Morsing, P. & Skøtt, O. 2003. Cyclooxygenase-2 contributes to elevated renin in the early postnatal period in rats. Am J Physiol Regul Integr Comp Physiol 284, R1179-R1189.
80. Stubbe, J., Madsen, K., Nielsen, F.T., Skøtt, O. & Jensen, B.L. 2006. Glucocorticoid impairs growth of the kidney outer medulla and accelerates loop of Henle differentiation and urinary concentrating capacity in rat kidney development. Am J Physiol Renal Physiol 291, F812-F822.
81. Stubbe, J., Madsen, K., Nielsen, F.T., Bonde, R.K., Skøtt, O. & Jensen, B.L. 2007. Postnatal adrenalectomy impairs urinary concentrating ability by increased COX-2 and leads to renal medullary injury. Am J Physiol Renal Physiol 293, F780-F789.
82. Suri, C., Jones, P.F., Patan, S., Bartunkova, S., Maisonpierre, P.C., Davis, S., Sato, T.N. & Yancopoulos, G.D. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180.
83. Takahashi, N., Chernavvsky, D.R., Gomez, R.A., Igarashi, P., Gitelman, H.J. & Smithies, O. 2000. Uncompensated polyuria in a mouse model of Bartter′s syndrome. Proc Natl Acad Sci USA 97, 5434-5439.
84. Tsuchida, S., Matsusaka, T., Chen, X., Okubo, S., Niimura, F., Nishimura, H., Fogo, A., Utsunomiya, H., Inagami, T. & Ichikawa, I. 1998. Murine double nullizygotes of the angiotensin type 1A and 1B receptor genes duplicate severe abnormal phenotypes of angiotensinogen nullizygotes. J Clin Invest 101, 755-760.
85. Tufro, A., Norwood, V.F., Carey, R.M. & Gomez, R.A. 1999. Vascular endothelial growth factor induces nephrogenesis and vasculogenesis. J Am Soc Nephrol 10, 2125-2134.
86. Tufro-McReddie, A., Harrison, J.K., Everett, A.D. & Gomez, R.A. 1993. Ontogeny of type 1 angiotensin II receptor gene expression in the rat. J Clin Invest 91, 530-537.
87. Tufro-McReddie, A., Romano, L.M., Harris, J.M., Ferder, L. & Gomez, R.A. 1995. Angiotensin II regulates nephrogenesis and renal vascular development. Am J Physiol 269, F110-F115.
88. Vehaskari, V.M., Aviles, D.H. & Manning, J. 2001. Prenatal programming of adult hypertension in the rat. Kidney Int 59, 238-245.
89. Wallace, K.B., Hook, J.B. & Bailie, M.D. 1980. Postnatal development of the renin-angiotensin system in rats. Am J Physiol 238, R432-R437.
90. Wolf, G., Ziyadeh, F.N., Helmchen, U., Zahner, G., Schroeder, R. & Stahl, R.A. 1995. ANG II is a mitogen for a murine cell line isolated from medullary thick ascending limb of Henle′s loop. Am J Physiol 268, F940-F947.
91. Woods, L.L. & Rasch, R. 1998. Perinatal ANG II programs adult blood pressure, glomerular number, and renal function in rats. Am J Physiol 275, R1593-R1599.
92. Woolf, A.S. 2004. Do kidney tubules serve an angiogenic soup? Kidney Int 66, 862-863.
93. Yasui, M., Marples, D., Belusa, R., Eklöf, A.C., Celsi, G., Nielsen, S. & Aperia, A. 1996. Development of urinary concentrating capacity: role of aquaporin-2. Am J Physiol 271, F461-F468.
94. Yim, H.E., Kim, J.H., Yoo, K.H., Bae, I.S., Hong, Y.S. & Lee, J.W. 2011. Spironolactone and enalapril differentially up-regulate the expression of VEGF and heme oxygenase-1 in the neonatal rat kidney. Pediatr Res 69, 378-383.
95. Yuan, H.T., Suri, C., Yancopoulos, G.D. & Woolf, A.S. 1999. Expression of angiopoietin-1, angiopoietin-2, and the Tie-2 receptor tyrosine kinase during mouse kidney maturation. J Am Soc Nephrol 10, 1722-1736.
96. Yuan, H.T., Suri, C., Landon, D.N., Yancopoulos, G.D. & Woolf, A.S. 2000. Angiopoietin-2 is a site-specific factor in differentiation of mouse renal vasculature. J Am Soc Nephrol 11, 1055-1066.