Sodium/hydrogen-exchanger-2 modulates colonocyte lineage differentiation.
NHE2
colonoids
intestinal differentiation
intestinal electrolyte transport
pHi regulation
sodium/hydrogen exchange
Journal
Acta physiologica (Oxford, England)
ISSN: 1748-1716
Titre abrégé: Acta Physiol (Oxf)
Pays: England
ID NLM: 101262545
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
revised:
12
10
2021
received:
18
06
2021
accepted:
01
01
2022
pubmed:
6
1
2022
medline:
30
4
2022
entrez:
5
1
2022
Statut:
ppublish
Résumé
The sodium/hydrogen exchanger 2 (NHE2) is an intestinal acid extruder with crypt-predominant localization and unresolved physiological significance. Our aim was to decipher its role in colonic epithelial cell proliferation, differentiation and electrolyte transport. Alterations induced by NHE2-deficiency were addressed in murine nhe2 pH The results suggest that NHE2 expression is activated when colonocytes emerge from the stem cell niche. Its activity increases progenitor cell pH
Substances chimiques
Slc26a3 protein, mouse
0
Slc9a2 protein, mouse
0
Sodium-Hydrogen Exchangers
0
Sulfate Transporters
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13774Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022 The Authors. Acta Physiologica published by John Wiley & Sons Ltd on behalf of Scandinavian Physiological Society.
Références
de Santa Barbara P, van den Brink GR, Roberts DJ. Development and differentiation of the intestinal epithelium. Cell Mol Life Sci. 2003;60:1322-1332.
Scoville DH, Sato T, He XC, Li L. Current view: intestinal stem cells and signaling. Gastroenterology. 2008;134:849-864.
Kay SK, Harrington HA, Shepherd S, et al. The role of the Hes1 crosstalk hub in Notch-Wnt interactions of the intestinal crypt. PLoS Comput Biol. 2017;13:e1005400.
Spit M, Koo BK, Maurice MM. Tales from the crypt: intestinal niche signals in tissue renewal, plasticity and cancer. Open Biol. 2018;8(9):180120. 10.1098/rsob.180120
Jensen J, Pedersen EE, Galante P, et al. Control of endodermal endocrine development by Hes-1. Nat Genet. 2000;24:36-44.
van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol. 2009;71:241-260.
Strubberg AM, Liu J, Walker NM, et al. Cftr modulates Wnt/β-catenin signaling and stem cell proliferation in murine intestine. Cell Mol Gastroenterol Hepatol. 2018;5:253-271.
Orlowski J, Grinstein S. Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch. 2004;447:549-565.
Kiela PR, Xu H, Ghishan FK. Apical NA+/H+ exchangers in the mammalian gastrointestinal tract. J Physiol Pharmacol. 2006;57(Suppl 7):51-79.
Dudeja PK, Rao DD, Syed I, et al. Intestinal distribution of human Na+/H+ exchanger isoforms NHE-1, NHE-2, and NHE-3 mRNA. Am J Physiol. 1996;271:G483-G493.
Guan Y, Dong J, Tackett L, Meyer JW, Shull GE, Montrose MH. NHE2 is the main apical NHE in mouse colonic crypts but an alternative Na+-dependent acid extrusion mechanism is upregulated in NHE2-null mice. Am J Physiol Gastrointest Liver Physiol. 2006;291:G689-G699.
Bachmann O, Riederer B, Rossmann H, et al. The Na+/H+ exchanger isoform 2 is the predominant NHE isoform in murine colonic crypts and its lack causes NHE3 upregulation. Am J Physiol Gastrointest Liver Physiol. 2004;287:G125-G133.
Wang Y, Kim R, Gunasekara DB, et al. Formation of human colonic crypt array by application of chemical gradients across a shaped epithelial monolayer. Cell Mol Gastroenterol Hepatol. 2018;5:113-130.
Yu Y, Seidler A, Zhou K, et al. Expression, localization and functional activity of the major Na(+)/H(+) exchange isoforms expressed in the intestinal cell line Caco-2BBe. Cell Physiol Biochem. 2019;52:1017-1038.
Alpers DH, Mahmood A, Engle M, Yamagishi F, DeSchryver-Kecskemeti K. The secretion of intestinal alkaline phosphatase (IAP) from the enterocyte. J Gastroenterol. 1994;29(Suppl 7):63-67.
Ueo T, Imayoshi I, Kobayashi T, et al. The role of Hes genes in intestinal development, homeostasis and tumor formation. Development. 2012;139:1071-1082.
Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science. 2001;294:2155-2158.
VanDussen KL, Samuelson LC. Mouse atonal homolog 1 directs intestinal progenitors to secretory cell rather than absorptive cell fate. Dev Biol. 2010;346:215-223.
van Es JH, de Geest N, van de Born M, Clevers H, Hassan BA. Intestinal stem cells lacking the Math1 tumour suppressor are refractory to Notch inhibitors. Nat Commun. 2010;1:18.
Gerbe F, van Es JH, Makrini L, et al. Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol. 2011;192:767-780.
Lee MG, Wigley WC, Zeng W, et al. Regulation of Cl−/HCO3−exchange by cystic fibrosis transmembrane conductance regulator expressed in NIH 3T3 and HEK 293 cells. J Biol Chem. 1999;274:3414-3421.
Jung J, Nam JH, Park HW, Oh U, Yoon JH, Lee MG. Dynamic modulation of ANO1/TMEM16A HCO3(-) permeability by Ca2+/calmodulin. Proc Natl Acad Sci USA. 2013;110:360-365.
Spencer AG, Labonte ED, Rosenbaum DP, et al. Intestinal inhibition of the Na+/H+ exchanger 3 prevents cardiorenal damage in rats and inhibits Na+ uptake in humans. Sci Transl Med. 2014;6:227ra236.
Zachos NC, Tse M, Donowitz M. Molecular physiology of intestinal Na+/H+ exchange. Annu Rev Physiol. 2005;67:411-443.
Kato A, Romero MF. Regulation of electroneutral NaCl absorption by the small intestine. Annu Rev Physiol. 2011;73:261-281.
Schultheis PJ, Clarke LL, Meneton P, et al. Targeted disruption of the murine Na+/H+ exchanger isoform 2 gene causes reduced viability of gastric parietal cells and loss of net acid secretion. J Clin Invest. 1998;101:1243-1253.
Ledoussal C, Woo AL, Miller ML, Shull GE. Loss of the NHE2 Na(+)/H(+) exchanger has no apparent effect on diarrheal state of NHE3-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1385-G1396.
Paehler Vor der Nolte A, Chodisetti G, Yuan Z, Busch F, Riederer B, Luo M, Yu Y, Menon MB, Schneider A, Stripecke R, Nikolovska K, Yeruva S, Seidler U. Na(+)/H(+) exchanger NHE1 and NHE2 have opposite effects on migration velocity in rat gastric surface cells. J Cell Physiol. 2017;232:1669-1680.
Shrode LD, Tapper H, Grinstein S. Role of intracellular pH in proliferation, transformation, and apoptosis. J Bioenerg Biomembr. 1997;29:393-399.
Stubbs M, McSheehy PM, Griffiths JR, Bashford CL. Causes and consequences of tumour acidity and implications for treatment. Mol Med Today. 2000;6:15-19.
Putney LK, Barber DL. Na-H exchange-dependent increase in intracellular pH times G2/M entry and transition. J Biol Chem. 2003;278:44645-44649.
Webb BA, Chimenti M, Jacobson MP, Barber DL. Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer. 2011;11:671-677.
Walker NM, Liu J, Stein SR, Stefanski CD, Strubberg AM, Clarke LL. Cellular chloride and bicarbonate retention alters intracellular pH regulation in Cftr KO crypt epithelium. Am J Physiol Gastrointest Liver Physiol. 2016;310:G70-G80.
Peterson MD, Bement WM, Mooseker MS. An in vitro model for the analysis of intestinal brush border assembly. II. Changes in expression and localization of brush border proteins during cell contact-induced brush border assembly in Caco-2BBe cells. J Cell Sci. 1993;105(Pt 2):461-472.
Matsumoto H, Erickson RH, Gum JR, Yoshioka M, Gum E, Kim YS. Biosynthesis of alkaline phosphatase during differentiation of the human colon cancer cell line Caco-2. Gastroenterology. 1990;98:1199-1207.
Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R. A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Biol Chem. 1995;270:8730-8738.
van Es JH, van Gijn ME, Riccio O, et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature. 2005;435:959-963.
Joseph C, Twombley K, Gattineni J, Zhang Q, Dwarakanath V, Baum M. Acid increases NHE8 surface expression and activity in NRK cells. Am J Physiol Renal Physiol. 2012;302:F495-F503.
Ulmschneider B, Grillo-Hill BK, Benitez M, Azimova DR, Barber DL, Nystul TG. Increased intracellular pH is necessary for adult epithelial and embryonic stem cell differentiation. J Cell Biol. 2016;215:345-355.
Liu Y, White KA, Barber DL. Intracellular pH regulates cancer and stem cell behaviors: a protein dynamics perspective. Front Oncol. 2020;10:1401. 10.3389/fonc.2020.01401
Yu FH, Shull GE, Orlowski J. Functional properties of the rat Na/H exchanger NHE-2 isoform expressed in Na/H exchanger-deficient Chinese hamster ovary cells. J Biol Chem. 1993;268:25536-25541.
Kapus A, Grinstein S, Wasan S, Kandasamy R, Orlowski J. Functional characterization of three isoforms of the Na+/H+ exchanger stably expressed in Chinese hamster ovary cells. ATP dependence, osmotic sensitivity, and role in cell proliferation. J Biol Chem. 1994;269:23544-23552.
Nunez M, Mayo KH, Starbuck C, Lauffenburger D. pH sensitivity of epidermal growth factor receptor complexes. J Cell Biochem. 1993;51:312-321.
Wang LX, Zhu F, Li JZ, et al. Epidermal growth factor promotes intestinal secretory cell differentiation in weaning piglets via Wnt/β-catenin signalling. Animal. 2020;14:790-798.
Gehart H, Clevers H. Tales from the crypt: new insights into intestinal stem cells. Nat Rev Gastroenterol Hepatol. 2019;16:19-34.
Stock C, Schwab A. Ion channels and transporters in metastasis. Biochim Biophys Acta. 1848;2638-2646:2015.
Macleod RJ. CaSR function in the intestine: Hormone secretion, electrolyte absorption and secretion, paracrine non-canonical Wnt signaling and colonic crypt cell proliferation. Best Pract Res Clin Endocrinol Metab. 2013;27:385-402.
Whitfield JF. The calcium-sensing receptor-a driver of colon cell differentiation. Curr Pharm Biotechnol. 2009;10:311-316.
Doroszewicz J, Waldegger P, Jeck N, Seyberth H, Waldegger S. pH dependence of extracellular calcium sensing receptor activity determined by a novel technique. Kidney Int. 2005;67:187-192.
Moeser AJ, Nighot PK, Ryan KA, Simpson JE, Clarke LL, Blikslager AT. Mice lacking the Na(+)/H(+) exchanger 2 have impaired recovery of intestinal barrier function. Am J Physiol Gastrointest Liver Physiol. 2008;295:G791-G797.
Aihara E, Matthis AL, Karns RA, et al. Epithelial regeneration after gastric ulceration causes prolonged cell-type alterations. Cell Mol Gastroenterol Hepatol. 2016;2:625-647.
Xue L, Aihara E, Wang TC, Montrose MH. Trefoil factor 2 requires Na/H exchanger 2 activity to enhance mouse gastric epithelial repair. J Biol Chem. 2011;286:38375-38382.
Singh AK, Liu Y, Riederer B, et al. Molecular transport machinery involved in orchestrating luminal acid-induced duodenal bicarbonate secretion in vivo. J Physiol. 2013;591:5377-5391.
Fujii M, Matano M, Toshimitsu K, et al. Human intestinal organoids maintain self-renewal capacity and cellular diversity in niche-inspired culture condition. Cell Stem Cell. 2018;23:787-793.e786.
Fernando EH, Dicay M, Stahl M, et al. A simple, cost-effective method for generating murine colonic 3D enteroids and 2D monolayers for studies of primary epithelial cell function. Am J Physiol Gastrointest Liver Physiol. 2017;313:G467-G475.
Bachmann O, Wuchner K, Rossmann H, et al. Expression and regulation of the Na+-K+-2Cl- cotransporter NKCC1 in the normal and CFTR-deficient murine colon. J Physiol. 2003;549:525-536.
Cinar A, Chen M, Riederer B, et al. NHE3 inhibition by cAMP and Ca2+ is abolished in PDZ-domain protein PDZK1-deficient murine enterocytes. J Physiol. 2007;581:1235-1246.
Yu Q, Liu X, Liu Y, et al. Defective small intestinal anion secretion, dipeptide absorption, and intestinal failure in suckling NBCe1-deficient mice. Pflugers Archiv. 2016;468:1419-1432.
Zucco F, Batto AF, Bises G, et al. An inter-laboratory study to evaluate the effects of medium composition on the differentiation and barrier function of Caco-2 cell lines. Altern Lab Anim. 2005;33:603-618.
Ferruzza S, Rossi C, Scarino ML, Sambuy Y. A protocol for in situ enzyme assays to assess the differentiation of human intestinal Caco-2 cells. Toxicol in Vitro. 2012;26:1247-1251.
Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA. 2008;105:15064-15069.
Xiao F, Yu Q, Li J, et al. Slc26a3 deficiency is associated with loss of colonic HCO3 (-) secretion, absence of a firm mucus layer and barrier impairment in mice. Acta Physiol (Oxf). 2014;211:161-175.
Xia W, Yu Q, Riederer B, et al. The distinct roles of anion transporters Slc26a3 (DRA) and Slc26a6 (PAT-1) in fluid and electrolyte absorption in the murine small intestine. Pflugers Arch. 2014;466:1541-1556.
Kini A, Singh AK, Riederer B, Yang I, Tan Q, di Stefano G, Tan Q, Xiao F, Xia W, Suerbaum S, Seidler U. Slc26a3 deletion alters pH-microclimate, mucin biosynthesis, microbiome composition and increases the TNFα expression in murine colon. Acta Physiol (Oxf). 2020;230:e13498.