Targeted mutagenesis of mitochondrial carbonic anhydrases VA and VB implicates both enzymes in ammonia detoxification and glucose metabolism

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 18, 2013, Pages 7423-7428

  Shah, Gul N ^a   Rubbelke, Timothy S ^a   Hendin, Joshua ^a   Nguyen, Hien ^a   Waheed, Abdul ^a   Shoemaker, James D ^a   Sly, William S ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anti obesity; Carbonic anhydrase V; Gene targeting; Hypoglycemia; Mouse model

Indexed keywords

AMMONIA; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE VA; CARBONATE DEHYDRATASE VB; CITRATE POTASSIUM SODIUM; DRINKING WATER; GLUCOSE; UNCLASSIFIED DRUG; WATER;

AMMONIA BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; FEMALE; GENE; GENE DISRUPTION; GENE MUTATION; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GROWTH; HYPERAMMONEMIA; LIVER; MALE; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROGENY; SURVIVAL; UREA CYCLE; WEANING; WILD TYPE;

AMMONIA; ANIMALS; BLOOD GLUCOSE; CARBONIC ANHYDRASE V; FEMALE; GENE TARGETING; GENOTYPE; GLUCOSE; MALE; METABOLIC DETOXICATION, DRUG; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MUTAGENESIS; RNA, MESSENGER; SURVIVAL ANALYSIS; WEIGHT GAIN;

ANIMALIA; MURINAE; MUS;

EID: 84876944140     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305805110     Document Type: Article

References (39)

1. Lindskog S, Silverman DN (2000) The Carbonic Anhydrases: New Horizons, eds Chegwidden WR, Carter ND, Edwards YH (Birkhauser, Basel, Switzerland), pp 175-195.
2. Sly WS, Hu PY (1995) Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu Rev Biochem 64:375-401.
3. Supuran CT (2008) Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7(2):168-181.
4. Hewett-Emmett D (2000) The Carbonic Anhydrases: New Horizons, eds Chegwidden WR, Carter ND, Edwards YH (Birkhauser, Basel, Switzerland), pp 29-76.
5. Lehtonen J, et al. (2004) Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J Biol Chem 279(4):2719-2727. (Pubitemid 38114261)
6. Fleming RE, et al. (1995) Carbonic anhydrase IV expression in rat and human gastrointestinal tract regional, cellular, and subcellular localization. J Clin Invest 96(6):2907-2913.
7. Pastoreková S, et al. (1997) Carbonic anhydrase IX, MN/CA IX: Analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts. Gastroenterology 112(2):398-408. (Pubitemid 27078826)
8. Kyllönen MS, et al. (2003) Localization of carbonic anhydrase XII to the basolateral membrane of H+-secreting cells of mouse and rat kidney. J Histochem Cytochem 51(9):1217-1224. (Pubitemid 37059533)
9. Parkkila S, et al. (2001) Expression of membrane-associated carbonic anhydrase XIV on neurons and axons in mouse and human brain. Proc Natl Acad Sci USA 98(4):1918-1923. (Pubitemid 32165598)
10. Hilvo M, et al. (2005) Characterization of CA XV, a new GPI-anchored form of carbonic anhydrase. Biochem J 392(Pt 1):83-92. (Pubitemid 41689404)
11. Leinonen J, Parkkila S, Kaunisto K, Koivunen P, Rajaniemi H (2001) Secretion of carbonic anhydrase isoenzyme VI (CA VI) from human and rat lingual serous von Ebner's glands. J Histochem Cytochem 49(5):657-662. (Pubitemid 32433505)
12. Shah GN, et al. (2000) Mitochondrial carbonic anhydrase CA VB: Differences in tissue distribution and pattern of evolution from those of CA VA suggest distinct physiological roles. Proc Natl Acad Sci USA 97(4):1677-1682. (Pubitemid 30118502)
13. Forster RE II, Dodgson SJ, Storey BT, Lin L (1984) Measurement of carbonic anhydrase activity inside cells and subcellular particles. Ann N Y Acad Sci 429:415-429. (Pubitemid 14085881)
14. Dodgson SJ, Forster RE II, Storey BT (1984) The role of carbonic anhydrase in hepatocyte metabolism. Ann N Y Acad Sci 429:516-524. (Pubitemid 14085892)
15. Dodgson SJ, Forster RE II (1986) Inhibition of CA V decreases glucose synthesis from pyruvate. Arch Biochem Biophys 251(1):198-204. (Pubitemid 17192998)
16. Dodgson SJ (1987) Inhibition of mitochondrial carbonic anhydrase and ureagenesis: A discrepancy examined. J Appl Physiol 63(5):2134-2141.
17. Hazen SA, Waheed A, Sly WS, LaNoue KF, Lynch CJ (1996) Differentiation-dependent expression of CA V and the role of carbonic anhydrase isozymes in pyruvate carboxylation in adipocytes. FASEB J 10(4):481-490. (Pubitemid 26120323)
18. Parkkila AK, et al. (1998) Expression of carbonic anhydrase V in pancreatic beta cells suggests role for mitochondrial carbonic anhydrase in insulin secretion. J Biol Chem 273(38):24620-24623.
19. Arechederra RL, Waheed A, Sly WS, Supuran CT, Minteer SD (2013) Effect of sulfonamides as carbonic anhydrase VA and VB inhibitors on mitochondrial metabolic energy conversion. Bioorg Med Chem 21(6):1544-1548.
20. Amor-Gueret M, Levi-Strauss M (1990) Nucleotide and derived amino-acid sequence of a cDNA encoding a new mouse carbonic anhydrase. Nucleic Acids Res 18(6):1646. (Pubitemid 20113864)
21. Nagao Y, et al. (1994) Mitochondrial carbonic anhydrase (isozyme V) in mouse and rat: cDNA cloning, expression, subcellular localization, processing, and tissue distribution. Proc Natl Acad Sci USA 91(22):10330-10334. (Pubitemid 24328990)
22. Nagao Y, Batanian JR, Clemente MF, Sly WS (1995) Genomic organization of the human gene (CA5) and pseudogene for mitochondrial carbonic anhydrase V and their localization to chromosomes 16q and 16p. Genomics 28(3):477-484.
23. Väänänen HK, Carter ND, Dodgson SJ (1991) Immunocytochemical localization of mitochondrial carbonic anhydrase in rat tissues. J Histochem Cytochem 39(4):451-459.
24. Harrison HE, Harrison HC (1955) Inhibition of urine citrate excretion and the production of renal calcinosis in the rat by acetazoleamide (diamox) administration. J Clin Invest 34(11):1662-1670.
25. Filippi L, et al. (2002) Pathogenic mechanism, prophylaxis, and therapy of symptomatic acidosis induced by acetazolamide. J Investig Med 50(2):125-132. (Pubitemid 34260399)
26. Ibrahim H, Lee YJ, Curthoys NP (2008) Renal response to metabolic acidosis: Role of mRNA stabilization. Kidney Int 73(1):11-18. (Pubitemid 350273636)
27. Braissant O, McLin VA, Cudalbu C (2012) Ammonia toxicity to the brain. J Inherit Metab Dis, 10.1007/s10545-012-9546-2.
28. Wolf B, et al. (1981) Multiple carboxylase deficiency: Clinical and biochemical improvement following neonatal biotin treatment. Pediatrics 68(1):113-118. (Pubitemid 11061376)
29. Lehninger AL, Carafoli E, Rossi CS (1967) Energy-linked ion movements in mitochondrial systems. Adv Enzymol Relat Areas Mol Biol 29:259-320.
30. Shah GN, et al. (2013) Pharmacological inhibition of mitochondrial carbonic anhydrases protects mouse cerebral pericytes from high glucose-induced oxidative stress and apoptosis. J Pharmacol Exp Ther 344(3):637-645.
31. Hazen SA, Waheed A, Sly WS, LaNoue KF, Lynch CJ (1997) Effect of carbonic anhydrase inhibition and acetoacetate on anaplerotic pyruvate carboxylase activity in cultured rat astrocytes. Dev Neurosci 19(2):162-171. (Pubitemid 27110639)
32. Bega D, Vaitkevicius H, Boland TA, Murray M, Chou SH (2012) Fatal hyperammonemic brain injury from valproic acid exposure. Case Rep Neurol 4(3):224-230.
33. Daniotti M, la Marca G, Fiorini P, Filippi L (2011) New developments in the treatment of hyperammonemia: Emerging use of carglumic acid. Int J Gen Med 4:21-28.
34. Price TO, Eranki V, Banks WA, Ercal N, Shah GN (2012) Topiramate treatment protects blood-brain barrier pericytes from hyperglycemia-induced oxidative damage in diabetic mice. Endocrinology 153(1):362-372.
35. Lynch CJ, et al. (1995) Role of hepatic carbonic anhydrase in de novo lipogenesis. Biochem J 310(Pt 1):197-202.
36. Supuran CT (2012) Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin Emerg Drugs 17(1):11-15.
37. Dodgson SJ, Cherian K (1989) Mitochondrial carbonic anhydrase is involved in rat renal glucose synthesis. Am J Physiol 257(6 Pt 1):E791-E796.
38. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680-685.
39. Shoemaker JD (2010) One-step metabolomics: Carbohydrates, organic and amino acids quantified in a single procedure. J Vis Exp (40):pii:2014. 10.3791/2014.