Reduced sodium/proton exchanger NHE3 activity causes congenital sodium diarrhea

Human Molecular Genetics

Volumn 24, Issue 23, 2015, Pages 6614-6623

  Janecke, Andreas R ^a   Heinz Erian, Peter ^a   Yin, Jianyi ^c   Petersen, Britt Sabina ^d   Franke, Andre ^d   Lechner, Silvia ^a   Fuchs, Irene ^a   Melancon, Serge ^e   Uhlig, Holm H ^f   Travis, Simon ^f   Marinier, Evelyne ^g   Perisic, Vojislav ^h   Ristic, Nina ^h   Gerner, Patrick ⁱ   Booth, Ian W ^j   Wedenoja, Satu ^k   Baumgartner, Nadja ^b   Vodopiutz, Julia ^l   Frechette Duval, Marie Christine ^m   De Lafollie, Jan ⁿ   Persad, Rabindranath ^o   Warner, Neil ^p   Ming Tse, C ^c   Sud, Karan ^c   Zachos, Nicholas C ^c   Sarker, Rafiquel ^c   Zhu, Xinjun ^q   Muise, Aleixo M ^p,r,s   Zimmer, Klaus Peter ⁿ   Witt, Heiko ^t   Zoller, Heinz ^b   Donowitz, Mark ^c   Müller, Thomas ^a   more..

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF KIEL   (Germany)

^e MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g HÔPITAL ROBERT DEBRÉ   (France)

^h UNIVERSITY CHILDREN S HOSPITAL   (Serbia)

ⁱ UNIVERSITY OF FREIBURG   (Germany)

^j UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^k UNIVERSITY OF HELSINKI   (Finland)

^l UNIV KLIN KINDER JUGENDHEILKUNDE   (Austria)

^m UNIVERSITY OF SHERBROOKE   (Canada)

ⁿ JUSTUS LIEBIG UNIVERSITY   (Germany)

^o UNIVERSITY OF ALBERTA   (Canada)

^p HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^q ALBANY MEDICAL CENTER   (United States)

^r UNIVERSITY OF TORONTO   (Canada)

^s UNIVERSITY OF TORONTO   (Canada)

^t TECHNICAL UNIVERSITY OF MUNICH   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

NATRIURETIC PEPTIDE RECEPTOR C; SERINE PEPTIDASE INHIBITOR KAZAL TYPE; SODIUM PROTON EXCHANGE PROTEIN 3; SODIUM PROTON EXCHANGE PROTEIN; SODIUM-HYDROGEN EXCHANGER 3;

ABDOMINAL DISTENSION; ADULT; ARTICLE; BIRTH WEIGHT; BLOOD PH; BODY HEIGHT; BODY WEIGHT; CASE REPORT; CHILD; CLINICAL ARTICLE; CONGENITAL SODIUM DIARRHEA; COPY NUMBER VARIATION; DIARRHEA; DNA SEQUENCING; FEMALE; GENE DELETION; GENE MUTATION; GENETIC SCREENING; HETEROZYGOSITY LOSS; HUMAN; IMMUNOBLOTTING; MALE; MICROARRAY ANALYSIS; MISSENSE MUTATION; NEWBORN; OSMOLALITY; POLYHYDRAMNIOS; PRESCHOOL CHILD; PROTEIN EXPRESSION; PS120 CELL LINE; QUANTITATIVE ANALYSIS; RNA SPLICING; SANGER SEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISM; SODIUM URINE LEVEL; UNIPARENTAL DISOMY; VERNER MORRISON SYNDROME; WHOLE EXOME SEQUENCING; YOUNG ADULT; ADOLESCENT; DNA MICROARRAY; DNA MUTATIONAL ANALYSIS; GENETICS; INBORN ERROR OF METABOLISM; INFANT; INFLAMMATORY BOWEL DISEASE; INTESTINE; METABOLISM; MICROVILLUS; MULTIPLE MALFORMATION SYNDROME; MUTATION; PATHOPHYSIOLOGY; RECESSIVE GENE;

ABNORMALITIES, MULTIPLE; ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; DIARRHEA; DNA MUTATIONAL ANALYSIS; FEMALE; GENES, RECESSIVE; HUMANS; INFANT; INFANT, NEWBORN; INFLAMMATORY BOWEL DISEASES; INTESTINES; MALE; METABOLISM, INBORN ERRORS; MICROVILLI; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SODIUM-HYDROGEN ANTIPORTER; YOUNG ADULT;

EID: 85016923853     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv367     Document Type: Article

References (38)

1. Berni Canani, R., Terrin, G., Cardillo, G., Tomaiuolo, R. and Castaldo, G. (2010) Congenital diarrheal disorders: improved understanding of gene defects is leading to advances in intestinal physiology and clinical management. J. Pediatr. Gastroenterol. Nutr., 50, 360–366.
2. Booth, I.W., Stange, G., Murer, H., Fenton, T.R. and Milla, P.J. (1985) Defective jejunal brush-border Na+/H+ exchange: a cause of congenital secretory diarrhoea. Lancet, 1, 1066–1069.
3. Holmberg, C. and Perheentupa, J. (1985) Congenital Na+ diarrhea: a new type of secretory diarrhea. J. Pediatr., 106, 56–61.
4. Muller, T., Wijmenga, C., Phillips, A.D., Janecke, A., Houwen, R.H., Fischer, H., Ellemunter, H., Fruhwirth, M., Offner, F., Hofer, S. et al. (2000) Congenital sodium diarrhea is an autosomal recessive disorder of sodium/proton exchange but unrelated to known candidate genes. Gastroenterology, 119, 1506–1513.
5. Keller, K.M., Wirth, S., Baumann, W., Sule, D. and Booth, I.W. (1990) Defective jejunal brush border membrane sodium/proton exchange in association with lethal familial protracted diarrhoea. Gut, 31, 1156–1158.
6. Fell, J.M., Miller, M.P., Finkel, Y. and Booth, I.W. (1992) Congenital sodium diarrhea with a partial defect in jejunal brush border membrane sodium transport, normal rectal transport, and resolving diarrhea. J. Pediatr. Gastroenterol. Nutr., 15, 112–116.
7. Heinz-Erian, P., Muller, T., Krabichler, B., Schranz, M., Becker, C., Ruschendorf, F., Nurnberg, P., Rossier, B., Vujic, M., Booth, I.W. et al. (2009) Mutations in SPINT2 cause a syndromic form of congenital sodium diarrhea. Am. J. Hum. Genet., 84, 188–196.
8. Salomon, J., Goulet, O., Canioni, D., Brousse, N., Lemale, J., Tounian, P., Coulomb, A., Marinier, E., Hugot, J.P., Ruemmele, F. et al. (2013) Genetic characterization of congenital tufting enteropathy: epcam associated phenotype and involvement of SPINT2 in the syndromic form. Hum. Genet., 133, 299–310.
9. Sivagnanam, M., Janecke, A.R., Muller, T., Heinz-Erian, P., Taylor, S. and Bird, L.M. (2010) Case of syndromic tufting enteropathy harbors SPINT2 mutation seen in congenital sodium diarrhea. Clin. Dysmorphol., 19, 48.
10. Sivagnanam, M., Mueller, J.L., Lee, H., Chen, Z., Nelson, S.F., Turner, D., Zlotkin, S.H., Pencharz, P.B., Ngan, B.Y., Libiger, O. et al. (2008) Identification of EpCAM as the gene for congenital tufting enteropathy. Gastroenterology, 135, 429–437.
11. Hoglund, P., Haila, S., Socha, J., Tomaszewski, L., Saarialho-Kere, U., Karjalainen-Lindsberg, M.L., Airola, K., Holmberg, C., de la Chapelle, A. and Kere, J. (1996) Mutations of the down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat. Genet., 14, 316–319.
12. Muller, T., Hess, M.W., Schiefermeier, N., Pfaller, K., Ebner, H. L., Heinz-Erian, P., Ponstingl, H., Partsch, J., Rollinghoff, B., Kohler, H. et al. (2008) MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat. Genet., 40, 1163–1165.
13. Wiegerinck, C.L., Janecke, A.R., Schneeberger, K., Vogel, G.F., van Haaften-Visser, D.Y., Escher, J.C., Adam, R., Thoni, C.E., Pfaller, K., Jordan, A.J. et al. (2014) Loss of syntaxin 3 causes variant microvillus inclusion disease. Gastroenterology, 147, 65–68 e10.
14. Fiskerstrand, T., Arshad, N., Haukanes, B.I., Tronstad, R.R., Pham, K.D., Johansson, S., Havik, B., Tonder, S.L., Levy, S.E., Brackman, D. et al. (2012) Familial diarrhea syndrome caused by an activating GUCY2C mutation. N. Engl. J. Med., 366, 1586–1595.
15. Müller, T., Rasool, I., Heinz-Erian, P., Mildenberger, E., Hülstrunk, C., Müller, A., Michaud, L., Koot, B.G.P., Ballauff, A., Vodopiutz, J. et al. (2015) Congenital Secretory Diarrhea caused by activating germline mutations in GUCY2C. Gut, doi: 10.1136/gutjnl-2015-309441.
16. Cha, B., Kim, J.H., Hut, H., Hogema, B.M., Nadarja, J., Zizak, M., Cavet, M., Lee-Kwon, W., Lohmann, S.M., Smolenski, A. et al. (2005) cGMP inhibition of Na+/H+ antiporter 3 (NHE3) requires PDZ domain adapter NHERF2, a broad specificity protein kinase G-anchoring protein. J. Biol. Chem., 280, 16642–16650.
17. Chen, T., Kocinsky, H.S., Cha, B., Murtazina, R., Yang, J., Tse, C. M., Singh, V., Cole, R., Aronson, P.S., de Jonge, H. et al. (2015) Cyclic GMP Kinase II (cGKII) inhibits NHE3 by altering its trafficking and phosphorylating NHE3 at three required sites: identification of a multifunctional phosphorylation site. J. Biol. Chem., 290, 1952–1965.
18. Donowitz, M., Mohan, S., Zhu, C.X., Chen, T.E., Lin, R., Cha, B., Zachos, N.C., Murtazina, R., Sarker, R. and Li, X. (2009) NHE3 regulatory complexes. J. Exp. Biol., 212, 1638–1646.
19. Cabado, A.G., Yu, F.H., Kapus, A., Lukacs, G., Grinstein, S. and Orlowski, J. (1996) Distinct structural domains confer cAMP sensitivity and ATP dependence to the Na+/H+ exchanger NHE3 isoform. J. Biol. Chem., 271, 3590–3599.
20. Murtazina, R., Kovbasnjuk, O., Donowitz, M. and Li, X. (2006) Na+/H+ exchanger NHE3 activity and trafficking are lipid Raft-dependent. J. Biol. Chem., 281, 17845–17855.
21. Schultheis, P.J., Clarke, L.L., Meneton, P., Miller, M.L., Soleimani, M., Gawenis, L.R., Riddle, T.M., Duffy, J.J., Doetschman, T., Wang, T. et al. (1998) Renal and intestinal absorptive defects in mice lacking the NHE3 Na+/H+ exchanger. Nat. Genet., 19, 282–285.
22. Noonan, W.T., Woo, A.L., Nieman, M.L., Prasad, V., Schultheis, P.J., Shull, G.E. and Lorenz, J.N. (2005) Blood pressure maintenance in NHE3-deficient mice with transgenic expression of NHE3 in small intestine. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R685–R691.
23. Arshad, N. and Visweswariah, S.S. (2012) The multiple and enigmatic roles of guanylyl cyclase C in intestinal homeostasis. FEBS Lett., 586, 2835–2840.
24. Padan, E. (2014) Functional and structural dynamics of NhaA, a prototype for Na(+) and H(+) antiporters, which are responsible for Na(+) and H(+) homeostasis in cells. Biochim. Biophys. Acta, 1837, 1047–1062.
25. Landau, M., Herz, K., Padan, E. and Ben-Tal, N. (2007) Model structure of the Na+/H+ exchanger 1 (NHE1): functional and clinical implications. J. Biol. Chem., 282, 37854–37863.
26. Lee, C., Yashiro, S., Dotson, D.L., Uzdavinys, P., Iwata, S., Sansom, M.S., von Ballmoos, C., Beckstein, O., Drew, D. and Cameron, A.D. (2014) Crystal structure of the sodium-proton antiporter NhaA dimer and new mechanistic insights. J. Gen. Physiol., 144, 529–544.
27. Anderson, C.A., Boucher, G., Lees, C.W., Franke, A., D’Amato, M., Taylor, K.D., Lee, J.C., Goyette, P., Imielinski, M., Latiano, A. et al. (2011) Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat. Genet., 43, 246–252.
28. Jostins, L., Ripke, S., Weersma, R.K., Duerr, R.H., McGovern, D. P., Hui, K.Y., Lee, J.C., Schumm, L.P., Sharma, Y., Anderson, C. A. et al. (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature, 491, 119–124.
29. Laubitz, D., Larmonier, C.B., Bai, A., Midura-Kiela, M.T., Lipko, M.A., Thurston, R.D., Kiela, P.R. and Ghishan, F.K. (2008) Colonic gene expression profile in NHE3-deficient mice: evidence for spontaneous distal colitis. Am. J. Physiol. Gastrointest. Liver Physiol., 295, G63–G77.
30. Larmonier, C.B., Laubitz, D., Hill, F.M., Shehab, K.W., Lipinski, L., Midura-Kiela, M.T., McFadden, R.M., Ramalingam, R., Hassan, K.A., Golebiewski, M. et al. (2013) Reduced colonic microbial diversity is associated with colitis in NHE3-deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol., 305, G667–G677.
31. Kiela, P.R., Laubitz, D., Larmonier, C.B., Midura-Kiela, M.T., Lipko, M.A., Janikashvili, N., Bai, A., Thurston, R. and Ghishan, F.K. (2009) Changes in mucosal homeostasis predispose NHE3 knockout mice to increased susceptibility to DSS-induced epithelial injury. Gastroenterology, 137, 965–975, 975 e961–910.
32. Sullivan, S., Alex, P., Dassopoulos, T., Zachos, N.C., Iacobuzio-Donahue, C., Donowitz, M., Brant, S.R., Cuffari, C., Harris, M. L., Datta, L.W. et al. (2009) Downregulation of sodium transporters and NHERF proteins in IBD patients and mouse colitis models: potential contributors to IBD-associated diarrhea. Inflamm. Bowel Dis., 15, 261–274.
33. Yeruva, S., Farkas, K., Hubricht, J., Rode, K., Riederer, B., Bachmann, O., Cinar, A., Rakonczay, Z., Molnar, T., Nagy, F. et al. (2010) Preserved Na(+)/H(+) exchanger isoform 3 expression and localization, but decreased NHE3 function indicate regulatory sodium transport defect in ulcerative colitis. Inflamm. Bowel Dis., 16, 1149–1161.
34. Zhu, X.C., Sarker, R., Horton, J.R., Chakraborty, M., Chen, T.E., Tse, C.M., Cha, B. and Donowitz, M. (2015) Nonsynonymous single nucleotide polymorphisms of NHE3 differentially decrease NHE3 transporter activity. Am. J. Physiol. Cell Physiol., 308, C758–C766.
35. Sarker, R., Valkhoff, V.E., Zachos, N.C., Lin, R., Cha, B., Chen, T. E., Guggino, S., Zizak, M., de Jonge, H., Hogema, B. et al. (2011) NHERF1 and NHERF2 are necessary for multiple but usually separate aspects of basal and acute regulation of NHE3 activity. Am. J. Physiol. Cell Physiol., 300, C771–C782.
36. Zachos, N.C., van Rossum, D.B., Li, X., Caraveo, G., Sarker, R., Cha, B., Mohan, S., Desiderio, S., Patterson, R.L. and Donowitz, M. (2009) Phospholipase C-gamma binds directly to the Na +/H+ exchanger 3 and is required for calcium regulation of exchange activity. J. Biol. Chem., 284, 19437–19444.
37. Zhu, X., Cha, B., Zachos, N.C., Sarker, R., Chakraborty, M., Chen, T.E., Kovbasnjuk, O. and Donowitz, M. (2011) Elevated calcium acutely regulates dynamic interactions of NHERF2 and NHE3 proteins in opossum kidney (OK) cell microvilli. J. Biol. Chem., 286, 34486–34496.
38. Levine, S.A., Montrose, M.H., Tse, C.M. and Donowitz, M. (1993) Kinetics and regulation of three cloned mammalian Na+/H+ exchangers stably expressed in a fibroblast cell line. J. Biol. Chem., 268, 25527–25535.