Deficiency in Six2 during prenatal development is associated with reduced nephron number, chronic renal failure, and hypertension in Br/+ adult mice

American Journal of Physiology - Renal Physiology

Volumn 296, Issue 5, 2009, Pages

  Fogelgren, Ben ^a   Yang, Shiming ^a   Sharp, Ian C ^a   Huckstep, Odaro J ^a   Ma, Wenbin ^c   Somponpun, S J ^b   Carlson, Edward C ^d   Uyehara, Catherine F T ^b   Lozanoff, Scott ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b TRIPLER ARMY MEDICAL CENTER   (United States)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^d UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Br mutant mouse; Glomerulus

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CREATININE; ENDOTHELIN 1; ENDOTHELIN A RECEPTOR; ENDOTHELIN B RECEPTOR; HOMEOBOX TRANSCRIPTION FACTOR SIX2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CHRONIC KIDNEY FAILURE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ELECTRON MICROSCOPY; FEMALE; GENE MUTATION; GLOMERULOPATHY; HYPERTENSION; IMMUNOHISTOCHEMISTRY; KIDNEY DEVELOPMENT; KIDNEY FUNCTION; KIDNEY HYPOPLASIA; MALE; MEAN ARTERIAL PRESSURE; MOUSE; NEPHRON; NONHUMAN; PATHOLOGICAL ANATOMY; PRIORITY JOURNAL; STEREOMETRY; ULTRASTRUCTURE ANALYSIS AND ELECTRON MICROSCOPY; URINARY EXCRETION;

EID: 66049099828     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.90550.2008     Document Type: Article

References (101)

1. K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis 39: S1-S266, 2002.
2. Alarcon VB, Marikawa Y. Molecular study of mouse peri-implantation development using the in vitro culture of aggregated inner cell mass. Mol Reprod Dev 67: 83-90, 2004. (Pubitemid 37467339)
3. Anderson S, Meyer TW, Rennke HG, Brenner BM. Control of glomerular hypertension limits glomerular injury in rats with reduced renal mass. J Clin Invest 76: 612-619, 1985. (Pubitemid 15227525)
4. Andreoli SP. Acute renal failure in the newborn. Semin Perinatol 28: 112-123, 2004.
5. Avner ED. Epithelial polarity and differentiation in polycystic kidney disease. J Cell Sci Suppl 17: 217-222, 1993.
6. Baddeley AJ, Gundersen HJ, Cruz-Orive LM. Estimation of surface area from vertical sections. J Microsc 142: 259-276, 1986.
7. Baldwin DS, Neugarten J. Hypertension and renal diseases. Am J Kidney Dis 10: 186-191, 1987.
8. Baur PS, Stacey TR. The use of PIPES buffer in the fixation of mammalian and marine tissues for electron microscopy. J Microsc 109: 315-327, 1977.
9. Benigni A. Defining the role of endothelins in renal pathophysiology on the basis of selective and unselective endothelin receptor antagonist studies. Curr Opin Nephrol Hypertens 4: 349-353, 1995.
10. Benigni A, Perico N, Gaspari F, Zoja C, Bellizzi L, Gabanelli M, Remuzzi G. Increased renal endothelin production in rats with reduced renal mass. Am J Physiol Renal Fluid Electrolyte Physiol 260: F331-F339, 1991.
11. Benigni A, Perico N, Remuzzi G. Endothelin antagonists and renal protection. J Cardiovasc Pharmacol 35: S75-S78, 2000.
12. Bidani AK, Griffin KA. Long-term renal consequences of hypertension for normal and diseased kidneys. Curr Opin Nephrol Hypertens 11: 73-80, 2002.
13. Bidani AK, Griffin KA, Picken M, Lansky DM. Continuous telemetric blood pressure monitoring and glomerular injury in the rat remnant kidney model. Am J Physiol Renal Fluid Electrolyte Physiol 265: F391-F398, 1993. (Pubitemid 23296538)
14. Bidani AK, Schwartz MM, Lewis EJ. Renal autoregulation and vulnerability to hypertensive injury in remnant kidney. Am J Physiol Renal Fluid Electrolyte Physiol 252: F1003-F1010, 1987.
15. Bird DN, Sato AK, Knee DS, Uyehara CF, Person DA, Claybaugh JR. Effects of prenatal ethanol exposure and sex on the arginine vasopressin response to hemorrhage in the rat. Am J Physiol Regul Integr Comp Physiol 291: R77-R82, 2006.
16. Bofill P, Goecke IA, Bonilla S, Alvo M, Marusic ET. Tissue-specific modulation of Na-K-ATPase alpha-subunit gene expression in uremic rats. Kidney Int 45: 672-678, 1994. (Pubitemid 24094477)
17. Boucher CA, Winchester CL, Hamilton GM, Winter AD, Johnson KJ, Bailey ME. Structure, mapping and expression of the human gene encoding the homeodomain protein, SIX2. Gene 247: 145-151, 2000.
18. Brenner BM. Nephron adaptation to renal injury or ablation. Am J Physiol Renal Fluid Electrolyte Physiol 249: F324-F337, 1985.
19. Brenner BM, Garcia DL, Anderson S. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens 1: 335-347, 1988. (Pubitemid 18269939)
20. Brodbeck S, Besenbeck B, Englert C. The transcription factor Six2 activates expression of the Gdnf gene as well as its own promoter. Mech Dev 121: 1211-1222, 2004. (Pubitemid 39141066)
21. Brodbeck S, Englert C. Genetic determination of nephrogenesis: the Pax/Eya/Six gene network. Pediatr Nephrol 19: 249-255, 2004. (Pubitemid 38313006)
22. Bruzzi I, Corna D, Zoja C, Orisio S, Schiffrin EL, Cavallotti D, Remuzzi G, Benigni A. Time course and localization of endothelin-1 gene expression in a model of renal disease progression. Am J Pathol 151: 1241-1247, 1997. (Pubitemid 27479753)
23. Carlson EC, Audette JL, Veitenheimer NJ, Risan JA, Laturnus DI, Epstein PN. Ultrastructural morphometry of capillary basement membrane thickness in normal and transgenic diabetic mice. Anat Rec A Discov Mol Cell Evol Biol 271: 332-341, 2003.
24. Carlson EC, Hinds D. Native banded collagen fibrils in the glomerular mesangial matrix of normal human and laboratory animals. J Ultrastruct Res 77: 241-247, 1981. (Pubitemid 12186422)
25. Clark AT, Bertram JF. Molecular regulation of nephron endowment. Am J Physiol Renal Physiol 276: F485-F497, 1999.
26. Coimbra TM, Carvalho J, Fattori A, Da Silva CG, Lachat JJ. Transforming growth factor-beta production during the development of renal fibrosis in rats with subtotal renal ablation. Int J Exp Pathol 77: 167-173, 1996. (Pubitemid 26341358)
27. Cullen-McEwen LA, Kett MM, Dowling J, Anderson WP, Bertram JF. Nephron number, renal function, and arterial pressure in aged GDNF heterozygous mice. Hypertension 41: 335-340, 2003. (Pubitemid 36204911)
28. Dhaun N, Goddard J, Webb DJ. The endothelin system and its antagonism in chronic kidney disease. J Am Soc Nephrol 17: 943-955, 2006.
29. Dische FE. Measurement of glomerular basement membrane thickness and its application to the diagnosis of thin-membrane nephropathy. Arch Pathol Lab Med 116: 43-49, 1992.
30. Dominiczak AF, Clark JS, Jeffs B, Anderson NH, Negrin CD, Lee WK, Brosnan MJ. Genetics of experimental hypertension. J Hypertens 16: 1859-1869, 1998. (Pubitemid 29002361)
31. Espinosa G, Lopez Farre A, Cernadas MR, Manzarbeitia F, Tan D, Digiuni E, Mosquera JR, Monton M, Millas I, Hernando L, Casado S, Caramelo C. Role of endothelin in the pathophysiology of renal ischemia-reperfusion in normal rabbits. Kidney Int 50: 776-782, 1996. (Pubitemid 26302665)
32. Faraj AH, Morley AR. Remnant kidney pathology after five-sixth nephrectomy in rat. I. A biochemical and morphological study. APMIS 100: 1097-1105, 1992.
33. Feiner HD, Katz LA, Gallo GR. Acquired cystic disease of kidney in chronic dialysis patients. Urology 17: 260-264, 1981.
34. Ferrandi M, Tripodi G, Salardi S, Florio M, Modica R, Barassi P, Parenti P, Shainskaya A, Karlish S, Bianchi G, Ferrari P. Renal Na,K-ATPase in genetic hypertension. Hypertension 28: 1018-1025, 1996. (Pubitemid 26415819)
35. Fogelgren B, Kuroyama MC, McBratney-Owen B, Spence AA, Malahn LE, Anawati MK, Cabatbat C, Alarcon VB, Marikawa Y, Lozanoff S. Misexpression of Six2 is associated with heritable frontonasal dysplasia and renal hypoplasia in 3H1 Br mice. Dev Dyn 237: 1767-1779, 2008.
36. Garg LC, Narang N, McArdle S. Na-K-ATPase in nephron segments of rats developing spontaneous hypertension. Am J Physiol Renal Fluid Electrolyte Physiol 249: F863-F869, 1985. (Pubitemid 16171221)
37. Glassberg KI, Stephens FD, Lebowitz RL, Braren V, Duckett JW, Jacobs EC, King LR, Perlmutter AD. Renal dysgenesis and cystic disease of the kidney: a report of the Committee on Terminology, Nomenclature and Classification, Section on Urology, American Academy of Pediatrics. J Urol 138: 1085-1092, 1987. (Pubitemid 17150831)
38. Granger JP, Abram S, Stec D, Chandler D, LaMarca B. Endothelin, the kidney, and hypertension. Curr Hypertens Rep 8: 298-303, 2006. (Pubitemid 44262925)
39. Grantham JJ. Polycystic kidney disease. I. Etiology and pathogenesis. Hosp Pract (Off Ed) 27: 51-59, 1992.
40. Greger R. Physiology of renal sodium transport. Am J Med Sci 319: 51-62, 2000. (Pubitemid 30367874)
41. Gretz NWR, Strauch M. The remnant kidney model. In: Experimental and Genetic Rat Models of Chronic Renal Failure, edited by Gretz NSM. Basel: Karger, 1993, p. 1-28.
42. Gundersen HJ. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R Thompson. J Microsc 143: 3-45, 1986.
43. Gundersen HJ, Jensen EB, Kieu K, Nielsen J. The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193: 199-211, 1999.
44. Hocher B, Thone-Reineke C, Rohmeiss P, Schmager F, Slowinski T, Burst V, Siegmund F, Quertermous T, Bauer C, Neumayer HH, Schleuning WD, Theuring F. Endothelin-1 transgenic mice develop glomerulosclerosis, interstitial fibrosis, and renal cysts but not hypertension. J Clin Invest 99: 1380-1389, 1997. (Pubitemid 27142776)
45. Hocher B, Zart R, Schwarz A, Vogt V, Braun C, Thone-Reineke C, Braun N, Neumayer HH, Koppenhagen K, Bauer C, Rohmeiss P. Renal endothelin system in polycystic kidney disease. J Am Soc Nephrol 9: 1169-1177, 1998. (Pubitemid 28283879)
46. Hoy WE, Douglas-Denton RN, Hughson MD, Cass A, Johnson K, Bertram JF. A stereological study of glomerular number and volume: preliminary findings in a multiracial study of kidneys at autopsy. Kidney Int Suppl 83: S31-S37, 2003. (Pubitemid 36126840)
47. Hughson M, Farris AB 3rd, Douglas-Denton R, Hoy WE, Bertram JF. Glomerular number and size in autopsy kidneys: the relationship to birth weight. Kidney Int 63: 2113-2122, 2003.
48. Jensen EB, Gundersen HJ, Osterby R. Determination of membrane thickness distribution from orthogonal intercepts. J Microsc 115: 19-33, 1979. (Pubitemid 10225698)
49. Kaddoura S, Curzen NP, Evans TW, Firth JD, Poole-Wilson PA. Tissue expression of endothelin-1 mRNA in endotoxaemia. Biochem Biophys Res Commun 218: 641-647, 1996. (Pubitemid 26050716)
50. Kawakami K, Sato S, Ozaki H, Ikeda K. Six family genes-structure and function as transcription factors and their roles in development. Bioessays 22: 616-626, 2000. (Pubitemid 30457953)
51. Keller G, Zimmer G, Mall G, Ritz E, Amann K. Nephron number in patients with primary hypertension. N Engl J Med 348: 101-108, 2003. (Pubitemid 36056716)
52. Kimmelstein P, Wilson C. Intercapillary lesions in the glomeruli of the kidney. Am J Clin Pathol 12: 83-97, 1936.
53. Knee DS, Sato AK, Uyehara CF, Claybaugh JR. Prenatal exposure to ethanol causes partial diabetes insipidus in adult rats. Am J Physiol Regul Integr Comp Physiol 287: R277-R283, 2004.
54. Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3: 169-181, 2008.
55. Kohan DE. Endothelins in the kidney: physiology and pathophysiology. Am J Kidney Dis 22: 493-510, 1993.
56. Kohan DE. The renal medullary endothelin system in control of sodium and water excretion and systemic blood pressure. Curr Opin Nephrol Hypertens 15: 34-40, 2006.
57. Lariviere R, Lebel M. Endothelin-1 in chronic renal failure and hypertension. Can J Physiol Pharmacol 81: 607-621, 2003. (Pubitemid 36836395)
58. Levine E. Acquired cystic kidney disease. Radiol Clin North Am 34: 947-964, 1996. (Pubitemid 26300133)
59. Lozanoff S. Midfacial retrusion in adult brachyrrhine mice. Acta Anat (Basel) 147: 125-132, 1993. (Pubitemid 23252472)
60. Lozanoff S, Johnston J, Ma W, Jourdan-Le Saux C. Immunohistochemical localization of Pax2 and associated proteins in the developing kidney of mice with renal hypoplasia. J Histochem Cytochem 49: 1081-1097, 2001. (Pubitemid 32800530)
61. Lozanoff S, Jureczek S, Feng T, Padwal R. Anterior cranial base morphology in mice with midfacial retrusion. Cleft Palate Craniofac J 31: 417-428, 1994. (Pubitemid 24367046)
62. Ma W, Lozanoff S. External craniofacial features, body size, and renal morphology in prenatal brachyrrhine mice. Teratology 47: 321-332, 1993. (Pubitemid 23117779)
63. Ma W, Lozanoff S. Morphological deficiency in the prenatal anterior cranial base of midfacially retrognathic mice. J Anat 188: 547-555, 1996.
64. Mackenzie HS, Brenner BM. Fewer nephrons at birth: a missing link in the etiology of essential hypertension? Am J Kidney Dis 26: 91-98, 1995.
65. Marasciulo FL, Montagnani M, Potenza MA. Endothelin-1: the yin and yang on vascular function. Curr Med Chem 13: 1655-1665, 2006. (Pubitemid 43821697)
66. Marikawa Y, Fujita TC, Alarcon VB. An enhancer-trap LacZ transgene reveals a distinct expression pattern of Kinesin family 26B in mouse embryos. Dev Genes Evol 214: 64-71, 2004. (Pubitemid 38324956)
67. Masaki T. The endothelin family: an overview. J Cardiovasc Pharmacol 35: S3-S5, 2000.
68. McBratney BM, Margaryan E, Ma W, Urban Z, Lozanoff S. Frontonasal dysplasia in 3H1 Br/Br mice. Anat Rec A Discov Mol Cell Evol Biol 271: 291-302, 2003. (Pubitemid 37238348)
69. Moscovici A, Bernheim J, Popovtzer MM, Rubinger D. Renal osteodystrophy in rats with reduced renal mass. Nephrol Dial Transplant 11, Suppl 3: 146-152, 1996.
70. Mouton P. Principles and Practices of Unbiased Stereology: An Introduction For Bioscientists. Baltimore, MD: Johns Hopkins University Press, 2002.
71. Nishimura DY, Searby CC, Alward WL, Walton D, Craig JE, Mackey DA, Kawase K, Kanis AB, Patil SR, Stone EM, Sheffield VC. A spectrum of FOXC1 mutations suggests gene dosage as a mechanism for developmental defects of the anterior chamber of the eye. Am J Hum Genet 68: 364-372, 2001. (Pubitemid 32147806)
72. Nyengaard JR, Bendtsen TF. Glomerular number and size in relation to age, kidney weight, and body surface in normal man. Anat Rec 232: 194-201, 1992.
73. Ogborn MR, Sareen S, Tomobe K, Takahashi H, Crocker JF. Renal tubule Na,K-ATPase polarity in different animal models of polycystic kidney disease. J Histochem Cytochem 43: 785-790, 1995.
74. Ohto H, Takizawa T, Saito T, Kobayashi M, Ikeda K, Kawakami K. Tissue and developmental distribution of Six family gene products. Int J Dev Biol 42: 141-148, 1998. (Pubitemid 28109375)
75. Oliver G, Wehr R, Jenkins NA, Copeland NG, Cheyette BN, Hartenstein V, Zipursky SL, Gruss P. Homeobox genes and connective tissue patterning. Development 121: 693-705, 1995.
76. Olson JL. Hypertension: essential and secondary forms. In: Heptinstall's Pathology of the Kidney (5th ed.), edited by Jennette JC, Olson JL, Schwartz MM, and Silva FG. Philadelphia: Lippincott-Raven, 1998, p. 943-1002.
77. Orisio S, Benigni A, Bruzzi I, Corna D, Perico N, Zoja C, Benatti L, Remuzzi G. Renal endothelin gene expression is increased in remnant kidney and correlates with disease progression. Kidney Int 43: 354-358, 1993. (Pubitemid 24063766)
78. Perazella MA, Khan S. Increased mortality in chronic kidney disease: a call to action. Am J Med Sci 331: 150-153, 2006.
79. Poladia DP, Kish K, Kutay B, Bauer J, Baum M, Bates CM. Link between reduced nephron number and hypertension: studies in a mutant mouse model. Pediatr Res 59: 489-493, 2006. (Pubitemid 43740044)
80. Pope JCT, Brock JW 3rd, Adams MC, Stephens FD, Ichikawa I. How they begin and how they end: classic and new theories for the development and deterioration of congenital anomalies of the kidney and urinary tract, CAKUT. J Am Soc Nephrol 10: 2018-2028, 1999.
81. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, McCullough PA, Kasiske BL, Kelepouris E, Klag MJ, Parfrey P, Pfeffer M, Raij L, Spinosa DJ, Wilson PW. Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 108: 2154-2169, 2003. (Pubitemid 37337595)
82. Schiffrin EL, Lariviere R, Li JS, Sventek P, Touyz RM. Deoxycorticosterone acetate plus salt induces overexpression of vascular endothelin-1 and severe vascular hypertrophy in spontaneously hypertensive rats. Hypertension 25: 769-773, 1995. (Pubitemid 26064483)
83. Schlager G. Kidney weight in mice: strain differences and genetic determination. J Hered 59: 171-174, 1968.
84. Schlager G. Selection for blood pressure levels in mice. Genetics 76: 537-549, 1974.
85. Schlager G, Sides J. Characterization of hypertensive and hypotensive inbred strains of mice. Lab Anim Sci 47: 288-292, 1997. (Pubitemid 127524102)
86. Schrier RW. Role of diminished renal function in cardiovascular mortality: marker or pathogenetic factor? J Am Coll Cardiol 47: 1-8, 2006.
87. Self M, Lagutin OV, Bowling B, Hendrix J, Cai Y, Dressler GR, Oliver G. Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J 25: 5214-5228, 2006. (Pubitemid 44658538)
88. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 93: 13176-13181, 1996. (Pubitemid 26382789)
89. Shimamura T, Morrison AB. A progressive glomerulosclerosis occurring in partial five-sixths nephrectomized rats. Am J Pathol 79: 95-106, 1975.
90. Shindo T, Kurihara H, Maemura K, Kurihara Y, Ueda O, Suzuki H, Kuwaki T, Ju KH, Wang Y, Ebihara A, Nishimatsu H, Moriyama N, Fukuda M, Akimoto Y, Hirano H, Morita H, Kumada M, Yazaki Y, Nagai R, Kimura K. Renal damage and salt-dependent hypertension in aged transgenic mice overexpressing endothelin-1. J Mol Med 80: 105-116, 2002. (Pubitemid 34169818)
91. Skou JC, Esmann M. The Na,K-ATPase. J Bioenerg Biomembr 24: 249-261, 1992.
92. Terzi F, Burtin M, Friedlander G. Using transgenic mice to analyze the mechanisms of progression of chronic renal failure. J Am Soc Nephrol 11, Suppl 16: S144-S148, 2000.
93. Theuring F, Thone-Reinecke C, Vogler H, Schmager F, Rohmeiss P, Slowinski T, Neumayer HH, Hocher B. Pathophysiology in endothelin-1 transgenic mice. J Cardiovasc Pharmacol 31, Suppl 1: S489-S491, 1998.
94. Van Esch H, Groenen P, Nesbit MA, Schuffenhauer S, Lichtner P, Vanderlinden G, Harding B, Beetz R, Bilous RW, Holdaway I, Shaw NJ, Fryns JP, Van de Ven W, Thakker RV, Devriendt K. GATA3 haploinsufficiency causes human HDR syndrome. Nature 406: 419-422, 2000. (Pubitemid 30625562)
95. Venable JH, Coggeshall R. A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25: 407-408, 1965.
96. Wilson PD. Epithelial cell polarity and disease. Am J Physiol Renal Physiol 272: F434-F442, 1997.
97. +-ATPase: mislocation to apical plasma membranes in polycystic kidney disease epithelia. Am J Physiol Renal Fluid Electrolyte Physiol 260: F420-F430, 1991.
98. Yang G, Merrill DC, Thompson MW, Robillard JE, Sigmund CD. Functional expression of the human angiotensinogen gene in transgenic mice. J Biol Chem 269: 32497-32502, 1994.
99. Yoshioka T, Shiraga H, Yoshida Y, Fogo A, Glick AD, Deen WM, Hoyer JR, Ichikawa I. "Intact nephrons" as the primary origin of proteinuria in chronic renal disease. Study in the rat model of subtotal nephrectomy. J Clin Invest 82: 1614-1623, 1988. (Pubitemid 19007766)
100. Zalups RK. The Os/+ mouse: a genetic animal model of reduced renal mass. Am J Physiol Renal Fluid Electrolyte Physiol 264: F53-F60, 1993.
101. Zhang HZ, Li P, Wang D, Huff S, Nimmakayalu M, Qumsiyeh M, Pober BR. FOXC1 gene deletion is associated with eye anomalies in ring chromosome 6. Am J Med Genet 124: 280-287, 2004. (Pubitemid 38082214)