Impaired renal function and development in Belgrade rats

American Journal of Physiology - Renal Physiology

Volumn 306, Issue 3, 2014, Pages

  Veuthey, Tania ^a   Hoffmann, Dana ^a   Vaidya, Vishal S ^a,b   Wessling Resnick, Marianne ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

DMT1; Iron deficiency anemia; Kidney; Renal development

Indexed keywords

ALBUMIN; CREATININE; FIBRINOGEN; IRON; KIDNEY INJURY MOLECULE 1; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; TRANSFERRIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPSY; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; ENZYME LINKED IMMUNOSORBENT ASSAY; GLOMERULUS FILTRATION; IMMUNOHISTOCHEMISTRY; IRON BLOOD LEVEL; KIDNEY DEVELOPMENT; KIDNEY FAILURE; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY MEDULLA; KIDNEY METABOLISM; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SCLEROSIS; WESTERN BLOTTING;

DMT1; IRON DEFICIENCY ANEMIA; KIDNEY; RENAL DEVELOPMENT;

ANIMALS; CATION TRANSPORT PROTEINS; CELL ADHESION MOLECULES; CREATININE; IRON; KIDNEY; LONGEVITY; MALE; RATS; RATS, INBRED F344; RENAL INSUFFICIENCY; TRANSFERRIN;

EID: 84893387250     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00285.2013     Document Type: Article

References (76)

1. Abouhamed M, Gburek J, Liu W, Torchalski B, Wilhelm A, Wolff NA, Christensen EI, Thevenod F, Smith CP. Divalent metal transporter 1 in the kidney proximal tubule is expressed in late endosomes/lysosomal membranes: implications for renal handling of protein-metal complexes. Am J Physiol Renal Physiol 290: F1525-F1533, 2006.
2. Al-Awqati Q, Preisig PA. Size does matter: will knockout of p21(WAF1/CIP1) save the kidney by limiting compensatory renal growth? Proc Natl Acad Sci USA 96: 10551-10553, 1999.
3. Andrews NC. Iron homeostasis: insights from genetics and animal models. Nat Rev Genet 1: 208-217, 2000.
4. Beierschmitt WP, Keenan KP, Weiner M. The development of acetaminophen-induced nephrotoxicity in male Fischer 344 rats of different ages. Arch Toxicol 59: 206-210, 1986.
5. Bennett WM, Porter GA. Endogenous creatinine clearance as a clinical measure of glomerular filtration rate. Br Med J 4: 84-86, 1971.
6. Bolignano D, Donato V, Coppolino G, Campo S, Buemi A, Lacquaniti A, Buemi M. Neutrophil gelatinase-associated lipocalin (NGAL) as a marker of kidney damage. Am J Kidney Dis 52: 595-605, 2008.
7. Brenner BM, Lawler EV, Mackenzie HS. The hyperfiltration theory: a paradigm shift in nephrology. Kidney Int 49: 1774-1777, 1996.
8. Chang YK, Lee SJ, Chung BH, Kim YO, Shin YS. Renal histology in patients with elevated serum creatinine and concurrent normal urinalysis. Clin Nephrol 77: 283-289, 2012.
9. Chockalingam UM, Murphy E, Ophoven JC, Weisdorf SA, Georgieff MK. Cord transferrin and ferritin values in newborn infants at risk for prenatal uteroplacental insufficiency and chronic hypoxia. J Pediatr 111: 283-286, 1987.
10. Christensen EI, Birn H. Megalin and cubilin: multifunctional endocytic receptors. Nat Rev Mol Cell Biol 3: 256-266, 2002.
11. Coca SG, Parikh CR. Urinary biomarkers for acute kidney injury: perspectives on translation. Clin J Am Soc Nephrol 3: 481-490, 2008.
12. de Zeeuw D, Parving HH, Henning RH. Microalbuminuria as an early marker for cardiovascular disease. J Am Soc Nephrol 17: 2100-2105, 2006.
13. Doolan PD, Alpen EL, Theil GB. A clinical appraisal of the plasma concentration and endogenous clearance of creatinine. Am J Med 32: 65-79, 1962.
14. Drake KA, Sauerbry MJ, Blohowiak SE, Repyak KS, Kling PJ. Iron deficiency and renal development in the newborn rat. Pediatr Res 66: 619-624, 2009.
15. Eddy AA. Experimental insights into the tubulointerstitial disease accompanying primary glomerular lesions. J Am Soc Nephrol 5: 1273-1287, 1994.
16. Enger E, Blegen EM. The relationship between endogenous creatinine clearance and serum creatinine in renal failure. Scand J Clin Lab Invest 16: 273-280, 1964.
17. Ferguson CJ, Wareing M, Delannoy M, Fenton R, McLarnon SJ, Ashton N, Cox AG, McMahon RF, Garrick LM, Green R, Smith CP, Riccardi D. Iron handling and gene expression of the divalent metal transporter, DMT1, in the kidney of the anemic Belgrade (b) rat. Kidney Int 64: 1755-1764, 2003.
18. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci USA 95: 1148-1153, 1998.
19. Fleming MD, Trenor CC 3rd, Su MA, Foernzler D, Beier DR, Dietrich WF, Andrews NC. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16: 383-386, 1997.
20. Frazer DM, Anderson GJ. Iron imports. I. Intestinal iron absorption and its regulation. Am J Physiol Gastrointest Liver Physiol 289: G631-G635, 2005.
21. Gambling L, Danzeisen R, Gair S, Lea RG, Charania Z, Solanky N, Joory KD, Srai SK, McArdle HJ. Effect of iron deficiency on placental transfer of iron and expression of iron transport proteins in vivo and in vitro. Biochem J 356: 883-889, 2001.
22. Ganz T. Macrophages and systemic iron homeostasis. J Innate Immun 4: 446-453, 2012.
23. Garrick M, Scott D, Walpole S, Finkelstein E, Whitbred J, Chopra S, Trivikram L, Mayes D, Rhodes D, Cabbagestalk K, Oklu R, Sadiq A, Mascia B, Hoke J, Garrick L. Iron supplementation moderates but does not cure the Belgrade anemia. Biometals 10: 65-76, 1997.
24. Georgieff MK, Wobken JK, Welle J, Burdo JR, Connor JR. Identification and localization of divalent metal transporter-1 (DMT-1) in term human placenta. Placenta 21: 799-804, 2000.
25. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488, 1997.
26. Han WK, Bonventre JV. Biologic markers for the early detection of acute kidney injury. Curr Opin Crit Care 10: 476-482, 2004.
27. Hinchliffe SA, Sargent PH, Chan YF, van Velzen D, Howard CV, Hutton JL, Rushton DI. "Medullary ray glomerular counting" as a method of assessment of human nephrogenesis. Pathol Res Pract 188: 775-782, 1992.
28. Horster MF, Braun GS, Huber SM. Embryonic renal epithelia: induction, nephrogenesis, and cell differentiation. Physiol Rev 79: 1157-1191, 1999.
29. Ichimura T, Hung CC, Yang SA, Stevens JL, Bonventre JV. Kidney injury molecule-1: a tissue and urinary biomarker for nephrotoxicantinduced renal injury. Am J Physiol Renal Physiol 286: F552-F563, 2004.
30. Jerums G, Panagiotopoulos S, Tsalamandris C, Allen TJ, Gilbert RE, Comper WD. Why is proteinuria such an important risk factor for progression in clinical trials? Kidney Int Suppl 63: S87-S92, 1997.
31. Jia X, Kim J, Veuthey T, Lee CH, Wessling-Resnick M. Glucose metabolism in the Belgrade rat, a model of iron-loading anemia. Am J Physiol Gastrointest Liver Physiol 304: G1095-G1102, 2013.
32. Kim J, Jia X, Buckett PD, Liu S, Lee CH, Wessling-Resnick M. Iron loading impairs lipoprotein lipase activity and promotes hypertriglyceridemia. FASEB J 27: 1657-1663, 2013.
33. Koji U, Masayoshi A, Rie K, Satoshi F. Comparison of hematology and blood chemistry parameters between Crj: CD(SD)IGS rats and BrlHan: WIST@Jcl(GALAS) rats. In: Biological Reference Data on CD(SD) IGS rats-2002/2003, edited by Yasuyuki M and Kazumoto S. Tokyo: Best Printing, 2002/2003, p. 48-52.
34. Kozyraki R, Fyfe J, Verroust PJ, Jacobsen C, Dautry-Varsat A, Gburek J, Willnow TE, Christensen EI, Moestrup SK. Megalindependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc Natl Acad Sci USA 98: 12491-12496, 2001.
35. Krishnamoorthy A, Ajay AK, Hoffmann D, Kim TM, Ramirez V, Campanholle G, Bobadilla NA, Waikar SS, Vaidya VS. Fibrinogen beta-derived Bbeta(15-42) peptide protects against kidney ischemia/reperfusion injury. Blood 118: 1934-1942, 2011.
36. Laboratories CRB. Baseline hematology and clinical chemistry values for charles river CD @ [CRL: CD@ (SD)BR] rats as a function of sex and age. In: Charles River Technical Bulletin. Wilmington, Massachusetts: The Charles River Breeding Laboratories, 1984, p. 4.
37. Legrand M, Payen D. Understanding urine output in critically ill patients. Ann Intensive Care 1: 13, 2011.
38. Levey AS. Measurement of renal function in chronic renal disease. Kidney Int 38: 167-184, 1990.
39. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of diet in renal disease study group. Ann Intern Med 130: 461-470, 1999.
40. Lisle SJ, Lewis RM, Petry CJ, Ozanne SE, Hales CN, Forhead AJ. Effect of maternal iron restriction during pregnancy on renal morphology in the adult rat offspring. Br J Nutr 90: 33-39, 2003.
41. Lote CJ, Harper L, Savage CO. Mechanisms of acute renal failure. Br J Anaesth 77: 82-89, 1996.
42. Luyckx VA, Brenner BM. The clinical importance of nephron mass. J Am Soc Nephrol 21: 898-910, 2010.
43. Mantle PG, Nicholls AW, Shockcor JP. H NMR spectroscopy-based metabolomic assessment of uremic toxicity, with toxicological outcomes, in male rats following an acute, mid-life insult from ochratoxin a. Toxins (Basel) 3: 504-519, 2011.
44. Marquez MG, Cabrera I, Serrano DJ, Sterin-Speziale N. Cell proliferation and morphometric changes in the rat kidney during postnatal development. Anat Embryol (Berl) 205: 431-440, 2002.
45. Merlet-Benichou C, Gilbert T, Muffat-Joly M, Lelievre-Pegorier M, Leroy B. Intrauterine growth retardation leads to a permanent nephron deficit in the rat. Pediatr Nephrol 8: 175-180, 1994.
46. Moulouel B, Houamel D, Delaby C, Tchernitchko D, Vaulont S, Letteron P, Thibaudeau O, Puy H, Gouya L, Beaumont C, Karim Z. Hepcidin regulates intrarenal iron handling at the distal nephron. Kidney Int 84: 756-766, 2013.
47. Muckenthaler MU, Galy B, Hentze MW. Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network. Annu Rev Nutr 28: 197-213, 2008.
48. Nankivell BJ. Creatinine clearance and the assessment of renal function. Australian Prescriber 24: 15-17, 2001.
49. Nguyen MT, Devarajan P. Biomarkers for the early detection of acute kidney injury. Pediatr Nephrol 23: 2151-2157, 2008.
50. Nickolas TL, Barasch J, Devarajan P. Biomarkers in acute and chronic kidney disease. Curr Opin Nephrol Hypertens 17: 127-132, 2008.
51. Rached E, Hoffmann D, Blumbach K, Weber K, Dekant W, Mally A. Evaluation of putative biomarkers of nephrotoxicity after exposure to ochratoxin a in vivo and in vitro. Toxicol Sci 103: 371-381, 2008.
52. Rodriguez MM, Gomez AH, Abitbol CL, Chandar JJ, Duara S, Zilleruelo GE. Histomorphometric analysis of postnatal glomerulogenesis in extremely preterm infants. Pediatr Dev Pathol 7: 17-25, 2004.
53. Rose B, Post TW. Clinical Physiology of Acid-Base and Electrolyte Disorders. New York, New York: McGraw Hill, 2001, p. 992.
54. Satchell SC, Tooke JE. What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 51: 714-725, 2008.
55. Schreuder MF, Wilhelm AJ, Bokenkamp A, Timmermans SM, Delemarre-van de Waal HA, van Wijk JA. Impact of gestational age and birth weight on amikacin clearance on day 1 of life. Clin J Am Soc Nephrol 4: 1774-1778, 2009.
56. Sieber M, Hoffmann D, Adler M, Vaidya VS, Clement M, Bonventre JV, Zidek N, Rached E, Amberg A, Callanan JJ, Dekant W, Mally A. Comparative analysis of novel noninvasive renal biomarkers and metabonomic changes in a rat model of gentamicin nephrotoxicity. Toxicol Sci 109: 336-349, 2009.
57. Sladic-Simic D, Martinovitch PN, Zivkovic N, Pavic D, Martinovic J, Kahn M, Ranney HM. A thalassemia-like disorder in Belgrade laboratory rats. Ann N Y Acad Sci 165: 93-99, 1969.
58. Sladic-Simic D, Zivkovic N, Pavic D, Marinkovic D, Martinovic J, Martinovitch PN. Hereditary hypochromic microcytic anemia in the laboratory rat. Genetics 53: 1079-1089, 1966.
59. Smith JC, Wilson LS. Study of a lifetime of sucrose intake by the Fischer-344 rat. Ann N Y Acad Sci 561: 291-306, 1989.
60. Stonestreet BS, Bell EF, Oh W. Validity of endogenous creatinine clearance in low birthweight infants. Pediatr Res 13: 1012-1014, 1979.
61. Sutherland MR, Gubhaju L, Moore L, Kent AL, Dahlstrom JE, Horne RS, Hoy WE, Bertram JF, Black MJ. Accelerated maturation and abnormal morphology in the preterm neonatal kidney. J Am Soc Nephrol 22: 1365-1374, 2011.
62. Sutherland MR, Yoder BA, McCurnin D, Seidner S, Gubhaju L, Clyman RI, Black MJ. Effects of ibuprofen treatment on the developing preterm baboon kidney. Am J Physiol Renal Physiol 302: F1286-F1292, 2012.
63. Thompson K, Molina RM, Brain JD, Wessling-Resnick M. Belgrade rats display liver iron loading. J Nutr 136: 3010-3014, 2006.
64. Thompson K, Molina RM, Donaghey T, Brain JD, Wessling-Resnick M. Iron absorption by Belgrade rat pups during lactation. Am J Physiol Gastrointest Liver Physiol 293: G640-G644, 2007.
65. Vaidya VS, Ozer JS, Dieterle F, Collings FB, Ramirez V, Troth S, Muniappa N, Thudium D, Gerhold D, Holder DJ, Bobadilla NA, Marrer E, Perentes E, Cordier A, Vonderscher J, Maurer G, Goering PL, Sistare FD, Bonventre JV. Kidney injury molecule-1 outperforms traditional biomarkers of kidney injury in preclinical biomarker qualification studies. Nat Biotechnol 28: 478-485, 2010.
66. Vaidya VS, Ramirez V, Ichimura T, Bobadilla NA, Bonventre JV. Urinary kidney injury molecule-1: a sensitive quantitative biomarker for early detection of kidney tubular injury. Am J Physiol Renal Physiol 290: F517-F529, 2006.
67. Vaidya VS, Shankar K, Lock EA, Dixon D, Mehendale HM. Molecular mechanisms of renal tissue repair in survival from acute renal tubule necrosis: role of ERK1/2 pathway. Toxicol Pathol 31: 604-618, 2003.
68. Vaidya VS, Waikar SS, Ferguson MA, Collings FB, Sunderland K, Gioules C, Bradwin G, Matsouaka R, Betensky RA, Curhan GC, Bonventre JV. Urinary biomarkers for sensitive and specific detection of acute kidney injury in humans. Clin Transl Sci 1: 200-208, 2008.
69. Vallon V. The proximal tubule in the pathophysiology of the diabetic kidney. Am J Physiol Regul Integr Comp Physiol 300: R1009-R1022, 2011.
70. Viau A, El Karoui K, Laouari D, Burtin M, Nguyen C, Mori K, Pillebout E, Berger T, Mak TW, Knebelmann B, Friedlander G, Barasch J, Terzi F. Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 120: 4065-4076, 2010.
71. Wang SN, Hirschberg R. Growth factor ultrafiltration in experimental diabetic nephropathy contributes to interstitial fibrosis. Am J Physiol Renal Physiol 278: F554-F560, 2000.
72. Wareing M, Ferguson CJ, Green R, Riccardi D, Smith CP. In vivo characterization of renal iron transport in the anaesthetized rat. J Physiol 524: 581-586, 2000.
73. Wessling-Resnick M. Iron imports. III. Transfer of iron from the mucosa into circulation. Am J Physiol Gastrointest Liver Physiol 290: G1-G6, 2006.
74. Wuhl E, Schaefer F. Managing kidney disease with blood-pressure control. Nat Rev Nephrol 7: 434-444, 2011.
75. Yang J, Goetz D, Li JY, Wang W, Mori K, Setlik D, Du T, Erdjument-Bromage H, Tempst P, Strong R, Barasch J. An iron delivery pathway mediated by a lipocalin. Mol Cell 10: 1045-1056, 2002.
76. Zandi-Nejad K, Luyckx VA, Brenner BM. Adult hypertension and kidney disease: the role of fetal programming. Hypertension 47: 502-508, 2006.