Acetazolamide Attenuates Lithium-Induced Nephrogenic Diabetes Insipidus.

To reduce lithium-induced nephrogenic diabetes insipidus (lithium-NDI), patients with bipolar disorder are treated with thiazide and amiloride, which are thought to induce antidiuresis by a compensatory increase in prourine uptake in proximal tubules. However, thiazides induced antidiuresis and alkalinized the urine in lithium-NDI mice lacking the sodium-chloride cotransporter, suggesting that inhibition of carbonic anhydrases (CAs) confers the beneficial thiazide effect. Therefore, we tested the effect of the CA-specific blocker acetazolamide in lithium-NDI. In collecting duct (mpkCCD) cells, acetazolamide reduced the cellular lithium content and attenuated lithium-induced downregulation of aquaporin-2 through a mechanism different from that of amiloride. Treatment of lithium-NDI mice with acetazolamide or thiazide/amiloride induced similar antidiuresis and increased urine osmolality and aquaporin-2 abundance. Thiazide/amiloride-treated mice showed hyponatremia, hyperkalemia, hypercalcemia, metabolic acidosis, and increased serum lithium concentrations, adverse effects previously observed in patients but not in acetazolamide-treated mice in this study. Furthermore, acetazolamide treatment reduced inulin clearance and cortical expression of sodium/hydrogen exchanger 3 and attenuated the increased expression of urinary PGE2 observed in lithium-NDI mice. These results show that the antidiuresis with acetazolamide was partially caused by a tubular-glomerular feedback response and reduced GFR. The tubular-glomerular feedback response and/or direct effect on collecting duct principal or intercalated cells may underlie the reduced urinary PGE2 levels with acetazolamide, thereby contributing to the attenuation of lithium-NDI. In conclusion, CA activity contributes to lithium-NDI development, and acetazolamide attenuates lithium-NDI development in mice similar to thiazide/amiloride but with fewer adverse effects.

[1]  N. Pastor-Soler,et al.  Collecting duct intercalated cell function and regulation. , 2015, Clinical journal of the American Society of Nephrology : CJASN.

[2]  P. Deen,et al.  Lithium causes G2 arrest of renal principal cells. , 2014, Journal of the American Society of Nephrology : JASN.

[3]  J. Wetzels,et al.  Hydrochlorothiazide attenuates lithium-induced nephrogenic diabetes insipidus independently of the sodium-chloride cotransporter. , 2014, American journal of physiology. Renal physiology.

[4]  C. Wagner,et al.  Renal β-intercalated cells maintain body fluid and electrolyte balance. , 2013, The Journal of clinical investigation.

[5]  G. Capasso,et al.  Evaluation of cellular plasticity in the collecting duct during recovery from lithium-induced nephrogenic diabetes insipidus. , 2013, American journal of physiology. Renal physiology.

[6]  P. Houillier,et al.  Overexpression of pendrin in intercalated cells produces chloride-sensitive hypertension. , 2013, Journal of the American Society of Nephrology : JASN.

[7]  R. Fenton,et al.  Is there a role for PGE2 in urinary concentration? , 2013, Journal of the American Society of Nephrology : JASN.

[8]  K. Shulman,et al.  The Effects of Lithium on Renal Function in Older Adults—A Systematic Review , 2012, Journal of geriatric psychiatry and neurology.

[9]  R. Chambrey,et al.  A new look at electrolyte transport in the distal tubule. , 2012, Annual review of physiology.

[10]  B. Palmer Metabolic complications associated with use of diuretics. , 2011, Seminars in nephrology.

[11]  C. Wagner,et al.  Proliferation of Acid-Secretory Cells in the Kidney during Adaptive Remodelling of the Collecting Duct , 2011, PloS one.

[12]  J. Stehle,et al.  alphaENaC-mediated lithium absorption promotes nephrogenic diabetes insipidus. , 2011, Journal of the American Society of Nephrology : JASN.

[13]  C. Supuran,et al.  Hyperchlorhidrosis caused by homozygous mutation in CA12, encoding carbonic anhydrase XII. , 2010, American journal of human genetics.

[14]  M. Maillard,et al.  Sodium and potassium balance depends on αENaC expression in connecting tubule. , 2010, Journal of the American Society of Nephrology : JASN.

[15]  P. Houillier,et al.  The Na+-dependent chloride-bicarbonate exchanger SLC4A8 mediates an electroneutral Na+ reabsorption process in the renal cortical collecting ducts of mice. , 2010, The Journal of clinical investigation.

[16]  R. Star,et al.  Major contribution of tubular secretion to creatinine clearance in mice. , 2010, Kidney international.

[17]  J. Fernández-Ramos,et al.  Nephrogenic diabetes insipidus: the key element of paradoxical hyponatremia , 2009, Pediatric nephrology (Berlin, West).

[18]  J. Wetzels,et al.  Amiloride blocks lithium entry through the sodium channel thereby attenuating the resultant nephrogenic diabetes insipidus. , 2009, Kidney international.

[19]  J. Grünfeld,et al.  Lithium nephrotoxicity revisited , 2009, Nature Reviews Nephrology.

[20]  D. Martin‐Coignard,et al.  Nephrogenic diabetes insipidus: treat with caution , 2009, Pediatric Nephrology.

[21]  G. Capasso,et al.  Pendrin in the mouse kidney is primarily regulated by Cl- excretion but also by systemic metabolic acidosis. , 2008, American journal of physiology. Cell physiology.

[22]  P. Quinton,et al.  Effect of Cytosolic pH on Epithelial Na+ Channel in Normal and Cystic Fibrosis Sweat Ducts , 2008, Journal of Membrane Biology.

[23]  P. Joyce,et al.  Lithium-induced nephrogenic diabetes insipidus: renal effects of amiloride. , 2008, Clinical journal of the American Society of Nephrology : CJASN.

[24]  G. Giebisch,et al.  Mouse model of type II Bartter's syndrome. II. Altered expression of renal sodium- and water-transporting proteins. , 2008, American journal of physiology. Renal physiology.

[25]  R. Walker,et al.  Amiloride restores renal medullary osmolytes in lithium-induced nephrogenic diabetes insipidus. , 2008, American journal of physiology. Renal physiology.

[26]  C. Musso,et al.  Creatinine reabsorption by the aged kidney , 2008, International Urology and Nephrology.

[27]  T. Kwon Dysregulation of Renal Cyclooxygenase-2 in Rats with Lithium-induced Nephrogenic Diabetes Insipidus , 2007, Electrolyte & blood pressure : E & BP.

[28]  G. Schwartz,et al.  The role of carbonic anhydrases in renal physiology. , 2007, Kidney international.

[29]  S. Nielsen,et al.  Lithium treatment induces a marked proliferation of primarily principal cells in rat kidney inner medullary collecting duct. , 2006, American journal of physiology. Renal physiology.

[30]  R. Blantz,et al.  Kidney oxygen consumption, carbonic anhydrase, and proton secretion. , 2006, American journal of physiology. Renal physiology.

[31]  P. Deen,et al.  Development of lithium-induced nephrogenic diabetes insipidus is dissociated from adenylyl cyclase activity. , 2006, Journal of the American Society of Nephrology : JASN.

[32]  J. Hoenderop,et al.  Acid-base status determines the renal expression of Ca2+ and Mg2+ transport proteins. , 2006, Journal of the American Society of Nephrology : JASN.

[33]  M. Knepper,et al.  Renal phenotype of UT-A urea transporter knockout mice. , 2005, Journal of the American Society of Nephrology : JASN.

[34]  V. Vallon,et al.  Enhanced passive Ca2+ reabsorption and reduced Mg2+ channel abundance explains thiazide-induced hypocalciuria and hypomagnesemia. , 2005, The Journal of clinical investigation.

[35]  R. Walker,et al.  Lithium-induced reduction in urinary concentrating ability and urinary aquaporin 2 (AQP2) excretion in healthy volunteers. , 2005, Kidney international.

[36]  S. Nielsen,et al.  Changes of Rat Kidney AQP2 and Na,K-ATPase mRNA Expression in Lithium-Induced Nephrogenic Diabetes insipidus , 2004, Nephron Experimental Nephrology.

[37]  J. Frøkiaer,et al.  Changes in cellular composition of kidney collecting duct cells in rats with lithium-induced NDI. , 2004, American journal of physiology. Cell physiology.

[38]  Min Zhao,et al.  Serial determination of glomerular filtration rate in conscious mice using FITC-inulin clearance. , 2004, American journal of physiology. Renal physiology.

[39]  D. Bichet,et al.  Reversed polarized delivery of an aquaporin-2 mutant causes dominant nephrogenic diabetes insipidus , 2003, The Journal of cell biology.

[40]  G. Shull,et al.  Downregulation of renal AQP2 water channel and NKCC2 in mice lacking the apical Na+‐H+ exchanger NHE3 , 2003, Journal of Physiology.

[41]  J. Frøkiaer,et al.  Altered expression of renal acid-base transporters in rats with lithium-induced NDI. , 2003, American journal of physiology. Renal physiology.

[42]  P. Remy,et al.  Chronic lithium nephropathy: MR imaging for diagnosis. , 2003, Radiology.

[43]  G. Giebisch,et al.  A rapid enzymatic method for the isolation of defined kidney tubule fragments from mouse , 2003, Pflügers Archiv.

[44]  A. Vandewalle,et al.  Long Term Regulation of Aquaporin-2 Expression in Vasopressin-responsive Renal Collecting Duct Principal Cells* , 2002, The Journal of Biological Chemistry.

[45]  G. Shull,et al.  Colonic H(+)-K(+)-ATPase in K(+) conservation and electrogenic Na(+) absorption during Na(+) restriction. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[46]  J. Schnermann Sodium transport deficiency and sodium balance in gene-targeted mice. , 2001, Acta Physiologica Scandinavica.

[47]  D. Brown,et al.  Remodeling the cellular profile of collecting ducts by chronic carbonic anhydrase inhibition. , 2001, American journal of physiology. Renal physiology.

[48]  M. Knepper,et al.  Profiling of renal tubule Na+ transporter abundances in NHE3 and NCC null mice using targeted proteomics , 2001, The Journal of physiology.

[49]  W. Sly,et al.  Expression of the Membrane-associated Carbonic Anhydrase Isozyme XII in the Human Kidney and Renal Tumors , 2000, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[50]  P. Deen,et al.  An impaired routing of wild‐type aquaporin‐2 after tetramerization with an aquaporin‐2 mutant explains dominant nephrogenic diabetes insipidus , 1999, The EMBO journal.

[51]  A. Hughes,et al.  Inhibition of carbonic anhydrase accounts for the direct vascular effects of hydrochlorothiazide. , 1999, Hypertension.

[52]  P. Lehenkari,et al.  Carbonic anhydrase II plays a major role in osteoclast differentiation and bone resorption by effecting the steady state intracellular pH and Ca2+. , 1998, Experimental cell research.

[53]  C. McHenry,et al.  Investigation of calcium-induced hydrolysis of phosphoinositides in normal and lithium-treated parathyroid cells. , 1995, American journal of surgery.

[54]  S. Nielsen,et al.  Lithium-induced downregulation of aquaporin-2 water channel expression in rat kidney medulla. , 1995, The Journal of clinical investigation.

[55]  N. Holstein-Rathlou,et al.  On determinants of glomerular filtration rate after inhibition of proximal tubular reabsorption. , 1994, The American journal of physiology.

[56]  S. Eiam-Ong,et al.  H-K-ATPase in distal renal tubular acidosis: urinary tract obstruction, lithium, and amiloride. , 1993, The American journal of physiology.

[57]  G. Rai,et al.  A study of plasma sodium levels in elderly people taking amiloride or triamterene in combination with hydrochlorothiazide. , 1993, Postgraduate medical journal.

[58]  N. Kurtzman,et al.  Effect of lithium and amiloride on collecting tubule transport enzymes. , 1992, The Journal of pharmacology and experimental therapeutics.

[59]  M. Meister,et al.  Lithium effects on dispersed bovine parathyroid cells grown in tissue culture. , 1991, Surgery.

[60]  G. Brown,et al.  Treatment of humoral hypercalcemia of malignancy in rats with inhibitors of carbonic anhydrase , 1990, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[61]  T. Mathew,et al.  Hyponatraemia due to the combination of hydrochlorothiazide and amiloride (Moduretic): Australian spontaneous reports 1977‐1988 , 1990, The Medical journal of Australia.

[62]  D. Batlle,et al.  Prevalence, pathogenesis, and treatment of renal dysfunction associated with chronic lithium therapy. , 1987, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[63]  G. Goodwin,et al.  The pharmacokinetic profile of lithium in rat and mouse; An important factor in psychopharmacological investigation of the drug , 1986, Neuropharmacology.

[64]  A. Bayer,et al.  Plasma electrolytes in elderly patients taking fixed combination diuretics. , 1986, Postgraduate medical journal.

[65]  E. Bárány,et al.  Carbonic anhydrase isoenzymes in the rat kidney. Effects of chronic acetazolamide treatment. , 1986, Acta physiologica Scandinavica.

[66]  D. Batlle,et al.  Amelioration of polyuria by amiloride in patients receiving long-term lithium therapy. , 1985, The New England journal of medicine.

[67]  L. Orci,et al.  Immunohistochemical localization of carbonic anhydrase in postnatal and adult rat kidney. , 1983, The American journal of physiology.

[68]  Anthony Martin,et al.  MALIGNANT HYPERKALAEMIA AFTER AMILORIDE/ HYDROCHLOROTHIAZIDE TREATMENT , 1981, The Lancet.

[69]  E. Brown,et al.  Lithium induces abnormal calcium-regulated PTH release in dispersed bovine parathyroid cells. , 1981, The Journal of clinical endocrinology and metabolism.

[70]  G. Johnson,et al.  Lithium nephrotoxicity. , 1981, The Medical journal of Australia.

[71]  D. Warnock,et al.  Effect of acetazolamide on bicarbonate reabsorption in the proximal tubule of the rat. , 1979, The American journal of physiology.

[72]  J. Arruda,et al.  On the mechanism of lithium-induced renal tubular acidosis. , 1977, The Journal of laboratory and clinical medicine.

[73]  R. Holman,et al.  INSULIN RATHER THAN GLUCOSE HOMŒOSTASIS IN THE PATHOPHYSIOLOGY OF DIABETES , 1976, The Lancet.

[74]  T. Maren,et al.  Carbonic anhydrase: chemistry, physiology, and inhibition. , 1967, Physiological reviews.