Defects in na+/glucose cotransporter (sglt1) trafficking and function cause glucose-galactose malabsorption

Defects in na+/glucose cotransporter (sglt1) trafficking and function cause glucose-galactose malabsorption

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ABSTRACT Cotransporters harness ion gradients to drive ‘active’ transport of substrates into cells, for example, the Na+/glucose cotransporter (SGLT1) couples sugar transport to Na+ gradients across the intestinal brush border1. Glucose-Galactose Malabsorption (GGM) is caused by a defect in SGLT1. The phenotype is neonatal onset of diarrhea that results in death unless these sugars are removed from the diet2–4. Previously we showed that two sisters with GGM had a missense mutation in the _SGLT1_ gene5. The gene has now been screened in 30 new patients, and a heterologous expression system has been used to link the mutations to the phenotype. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal Receive 12 print issues and online access $209.00 per year only $17.42 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS ENTEROENDOCRINE CELLS COUPLE NUTRIENT SENSING TO NUTRIENT ABSORPTION BY REGULATING ION TRANSPORT Article Open access 22 September 2020 STRUCTURE AND MECHANISM OF THE SGLT FAMILY OF GLUCOSE TRANSPORTERS Article 08 December 2021 STRUCTURE AND THIAZIDE INHIBITION MECHANISM OF THE HUMAN NA–CL COTRANSPORTER Article 15 February 2023 REFERENCES * Wright, E.M., Hirayama, B.A., Loo, D.D.F., Turk, E & Hager, K. Intestinal Sugar Transport. In _Physiology of the Gastrointestinal Tract_, (ed. Johnson, L.R.)1751–1772 (New York, Raven, 1994). Google Scholar  * Lindquist, B. & Meeuwisse, G.W. Chronic diarrhoea caused by monosaccharide malabsorption. _Acta Paediatrica_ 51, 674–685 (1962). Article  CAS  Google Scholar  * Laplane, R., Polonovski, C., Etienne, M., Debray, P., Lods, J.C. & Pissaro, B. L'intolerance aux sucres a transfert intestinal actif Ses rapports avec l'intolerance au lactose et le syndrome coeliaque. _Arch. Fr. Pediatr._ 19, 895 (1962). Google Scholar  * Desjeux, J.-R., Turk, E. & Wright, E.M., Na+D-Glucose cotransport defects leading to renal glycosuria and congenital selective intestinal malabsorption of glucose and galactose. In _Metabolic Basis of Inherited Disease_, Vol. 3 (eds Scriver, C.R., Beaudet, A.L. & Sly, W.S.) 3563–3580 (New York, McGraw-Hill, 1995). Google Scholar  * Turk, E., Zabel, B., Mundlos, S., Dyer, J. & Wright, E.M. Glucose/galactose malabsorption caused by a defect in the Na+/glucose cotransporter. _Nature_ 350, 354–356 (1991). Article  CAS  Google Scholar  * Loo, D.D.F., Hazama, A., Supplisson, S., Turk, E. & Wright, E.M. Relaxation kinetics of the Na+/glucose cotransporter. _Proc. Natl. Acad. Sci. USA_ 90, 5767–5771 (1993). Article  CAS  Google Scholar  * Zampighi, G.A. _et al_. A method for determining the unitary functional capacity of cloned channels and transporters expressed in Xenopus laevis oocytes. _J. Mem. Biol._ 148, 65–78 (1995). Article  CAS  Google Scholar  * Mount, S.M. A Catalogue of Splice Junction Sequences. _Nucl Acids Res._ 10, 459–473 (1982). Article  CAS  Google Scholar  * Panayotova-Heiermann, M., Loo, D.D.F., Lostao, M.P. & Wright, E.M. Sodium/D-glucose cotransporter charge movements involve polar residues. _J. Biol. Chem._ 269, 21016–21020 (1994). CAS  PubMed  Google Scholar  * Hediger, M.A., Coady, M.J., Ikeda, T.S. & Wright, E.M. Expression cloning and cDNA sequencing of the Na+/glucose cotransporter. _Nature_ 330, 379–381 (1987). Article  CAS  Google Scholar  * Mackenzie, B., Panayotova-Heiermann, M., Loo, D.D.F., Lever, J.E. & Wright, E.M. SAAT1 is a low affinity NaVglucose cotransporter and not an amino acid transporterA interpretation. _J. Biol. Chem._ 269, 22488–22491 (1994). CAS  PubMed  Google Scholar  * Kwon, H.M., Yamauchi, A., Uchida, S., Preston, A.S., Garcia-Perez, A., Burg, M.B. & Handler, J.S. Cloning of the cDNA of Na+/myo-inositol cotransporter, a hypertoncity stress protein. _J. Biol. Chem._ 6297–6301 (1992). * Stirling, C.E., Schneider, A.J., Wong, M.-D. & Kinter, W.B. Quantitative radioqutography of sugar transport in intestinal biopsies from normal humans and a patient with glucose-galactose malabsorption. _J.Clin. Invest._ 51, 438–451 (1972). Article  CAS  Google Scholar  * Lostao, M.P., Hirayama, B.A., Panayotova-Heiermann, M., Sampogna, S.L., Bok, D. & Wright, E.M. Arginine-427 in the Na/glucose cotransporter (SGLT1) is involved in trafficking to the plasma membrane. _FEES Lett._ 377, 181–184 (1995). Article  CAS  Google Scholar  * Turk, E., Martín, M.G. & Wright, E.M. Structure of the human NaVglucose cotransporter gene SGLTl. _J. Biol. Chem._ 269, 15204–15209 (1994). CAS  PubMed  Google Scholar  * Orita, M., Suzuki, Y., Sekiya, T. & Hayashi, K. Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction. _Genomics_ 5, 874–879 (1989). Article  CAS  Google Scholar  * Higuchi, R.B., Krummel, B. & Saiki, R.K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions._Nucl. Acids Res._ 16, 7351–7367 (1986). Article  Google Scholar  * Ikeda, T.S., Hwang, E.S., Coady, M.J., Hirayama, B.A., Hediger, M.A. & Wright, E.M. Characterization of a Na+/glucose cotransporter cloned from rabbit small intestine. _J. Mem. Biol._ 110, 87–95 (1989). Article  CAS  Google Scholar  * Hirayama, B.A. and Wright, E.M. Glycosylation of the rabbit intestinal brush border Na+/glucose cotransporter. _Biochim. Biophys. Acta_ 1103, 37–44 (1992). Article  CAS  Google Scholar  * Parent, L., Supplisson, S., Loo, D.D.F. & Wright, E.M. Electrogenic properties of the cloned Na+/glucose cotransporter: I Voltage-Clamp studies. _J. Mem. Biol._ 125, 49–62 (1992). CAS  Google Scholar  * Turk, E., Kerner, C.J., Lostao, M.P. & Wright, E.M., Topology of the Human Na+/glucose Cotransporter SGLT1. _J Biol. Chem._ 271, 1925–1934 (1996). Article  CAS  Google Scholar  * Krawczak, M., Reiss, J. & Cooper, D.N. The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes and consequences. _Hum. Genet._ 90, 41–54 (1992). Article  CAS  Google Scholar  Download references AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Departments of Physiology and Pediatrics, UCLA School of Medicine, Los Angeles, California, 90095-1751, USA Martín G. Martín, Eric Turk, M. Pilar Lostao, Cynthia Kerner & Ernest M. Wright Authors * Martín G. Martín View author publications You can also search for this author inPubMed Google Scholar * Eric Turk View author publications You can also search for this author inPubMed Google Scholar * M. Pilar Lostao View author publications You can also search for this author inPubMed Google Scholar * Cynthia Kerner View author publications You can also search for this author inPubMed Google Scholar * Ernest M. Wright View author publications You can also search for this author inPubMed Google Scholar RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Martín, M., Turk, E., Lostao, M. _et al._ Defects in Na+/glucose cotransporter (SGLT1) trafficking and function cause glucose-galactose malabsorption. _Nat Genet_ 12, 216–220 (1996). https://doi.org/10.1038/ng0296-216 Download citation * Received: 11 September 1995 * Accepted: 22 November 1995 * Issue Date: 01 February 1996 * DOI: https://doi.org/10.1038/ng0296-216 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative

ABSTRACT Cotransporters harness ion gradients to drive ‘active’ transport of substrates into cells, for example, the Na+/glucose cotransporter (SGLT1) couples sugar transport to Na+


gradients across the intestinal brush border1. Glucose-Galactose Malabsorption (GGM) is caused by a defect in SGLT1. The phenotype is neonatal onset of diarrhea that results in death unless


these sugars are removed from the diet2–4. Previously we showed that two sisters with GGM had a missense mutation in the _SGLT1_ gene5. The gene has now been screened in 30 new patients, and


a heterologous expression system has been used to link the mutations to the phenotype. Access through your institution Buy or subscribe This is a preview of subscription content, access via


your institution ACCESS OPTIONS Access through your institution Subscribe to this journal Receive 12 print issues and online access $209.00 per year only $17.42 per issue Learn more Buy


this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: *


Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS ENTEROENDOCRINE CELLS COUPLE NUTRIENT SENSING TO NUTRIENT


ABSORPTION BY REGULATING ION TRANSPORT Article Open access 22 September 2020 STRUCTURE AND MECHANISM OF THE SGLT FAMILY OF GLUCOSE TRANSPORTERS Article 08 December 2021 STRUCTURE AND


THIAZIDE INHIBITION MECHANISM OF THE HUMAN NA–CL COTRANSPORTER Article 15 February 2023 REFERENCES * Wright, E.M., Hirayama, B.A., Loo, D.D.F., Turk, E & Hager, K. Intestinal Sugar


Transport. In _Physiology of the Gastrointestinal Tract_, (ed. Johnson, L.R.)1751–1772 (New York, Raven, 1994). Google Scholar  * Lindquist, B. & Meeuwisse, G.W. Chronic diarrhoea caused


by monosaccharide malabsorption. _Acta Paediatrica_ 51, 674–685 (1962). Article  CAS  Google Scholar  * Laplane, R., Polonovski, C., Etienne, M., Debray, P., Lods, J.C. & Pissaro, B.


L'intolerance aux sucres a transfert intestinal actif Ses rapports avec l'intolerance au lactose et le syndrome coeliaque. _Arch. Fr. Pediatr._ 19, 895 (1962). Google Scholar  *


Desjeux, J.-R., Turk, E. & Wright, E.M., Na+D-Glucose cotransport defects leading to renal glycosuria and congenital selective intestinal malabsorption of glucose and galactose. In


_Metabolic Basis of Inherited Disease_, Vol. 3 (eds Scriver, C.R., Beaudet, A.L. & Sly, W.S.) 3563–3580 (New York, McGraw-Hill, 1995). Google Scholar  * Turk, E., Zabel, B., Mundlos, S.,


Dyer, J. & Wright, E.M. Glucose/galactose malabsorption caused by a defect in the Na+/glucose cotransporter. _Nature_ 350, 354–356 (1991). Article  CAS  Google Scholar  * Loo, D.D.F.,


Hazama, A., Supplisson, S., Turk, E. & Wright, E.M. Relaxation kinetics of the Na+/glucose cotransporter. _Proc. Natl. Acad. Sci. USA_ 90, 5767–5771 (1993). Article  CAS  Google Scholar


  * Zampighi, G.A. _et al_. A method for determining the unitary functional capacity of cloned channels and transporters expressed in Xenopus laevis oocytes. _J. Mem. Biol._ 148, 65–78


(1995). Article  CAS  Google Scholar  * Mount, S.M. A Catalogue of Splice Junction Sequences. _Nucl Acids Res._ 10, 459–473 (1982). Article  CAS  Google Scholar  * Panayotova-Heiermann, M.,


Loo, D.D.F., Lostao, M.P. & Wright, E.M. Sodium/D-glucose cotransporter charge movements involve polar residues. _J. Biol. Chem._ 269, 21016–21020 (1994). CAS  PubMed  Google Scholar  *


Hediger, M.A., Coady, M.J., Ikeda, T.S. & Wright, E.M. Expression cloning and cDNA sequencing of the Na+/glucose cotransporter. _Nature_ 330, 379–381 (1987). Article  CAS  Google Scholar


  * Mackenzie, B., Panayotova-Heiermann, M., Loo, D.D.F., Lever, J.E. & Wright, E.M. SAAT1 is a low affinity NaVglucose cotransporter and not an amino acid transporterA interpretation.


_J. Biol. Chem._ 269, 22488–22491 (1994). CAS  PubMed  Google Scholar  * Kwon, H.M., Yamauchi, A., Uchida, S., Preston, A.S., Garcia-Perez, A., Burg, M.B. & Handler, J.S. Cloning of the


cDNA of Na+/myo-inositol cotransporter, a hypertoncity stress protein. _J. Biol. Chem._ 6297–6301 (1992). * Stirling, C.E., Schneider, A.J., Wong, M.-D. & Kinter, W.B. Quantitative


radioqutography of sugar transport in intestinal biopsies from normal humans and a patient with glucose-galactose malabsorption. _J.Clin. Invest._ 51, 438–451 (1972). Article  CAS  Google


Scholar  * Lostao, M.P., Hirayama, B.A., Panayotova-Heiermann, M., Sampogna, S.L., Bok, D. & Wright, E.M. Arginine-427 in the Na/glucose cotransporter (SGLT1) is involved in trafficking


to the plasma membrane. _FEES Lett._ 377, 181–184 (1995). Article  CAS  Google Scholar  * Turk, E., Martín, M.G. & Wright, E.M. Structure of the human NaVglucose cotransporter gene


SGLTl. _J. Biol. Chem._ 269, 15204–15209 (1994). CAS  PubMed  Google Scholar  * Orita, M., Suzuki, Y., Sekiya, T. & Hayashi, K. Rapid and sensitive detection of point mutations and DNA


polymorphisms using the polymerase chain reaction. _Genomics_ 5, 874–879 (1989). Article  CAS  Google Scholar  * Higuchi, R.B., Krummel, B. & Saiki, R.K. A general method of in vitro


preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions._Nucl. Acids Res._ 16, 7351–7367 (1986). Article  Google Scholar  * Ikeda, T.S., Hwang, E.S.,


Coady, M.J., Hirayama, B.A., Hediger, M.A. & Wright, E.M. Characterization of a Na+/glucose cotransporter cloned from rabbit small intestine. _J. Mem. Biol._ 110, 87–95 (1989). Article 


CAS  Google Scholar  * Hirayama, B.A. and Wright, E.M. Glycosylation of the rabbit intestinal brush border Na+/glucose cotransporter. _Biochim. Biophys. Acta_ 1103, 37–44 (1992). Article 


CAS  Google Scholar  * Parent, L., Supplisson, S., Loo, D.D.F. & Wright, E.M. Electrogenic properties of the cloned Na+/glucose cotransporter: I Voltage-Clamp studies. _J. Mem. Biol._


125, 49–62 (1992). CAS  Google Scholar  * Turk, E., Kerner, C.J., Lostao, M.P. & Wright, E.M., Topology of the Human Na+/glucose Cotransporter SGLT1. _J Biol. Chem._ 271, 1925–1934


(1996). Article  CAS  Google Scholar  * Krawczak, M., Reiss, J. & Cooper, D.N. The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes


and consequences. _Hum. Genet._ 90, 41–54 (1992). Article  CAS  Google Scholar  Download references AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Departments of Physiology and Pediatrics,


UCLA School of Medicine, Los Angeles, California, 90095-1751, USA Martín G. Martín, Eric Turk, M. Pilar Lostao, Cynthia Kerner & Ernest M. Wright Authors * Martín G. Martín View author


publications You can also search for this author inPubMed Google Scholar * Eric Turk View author publications You can also search for this author inPubMed Google Scholar * M. Pilar Lostao


View author publications You can also search for this author inPubMed Google Scholar * Cynthia Kerner View author publications You can also search for this author inPubMed Google Scholar *


Ernest M. Wright View author publications You can also search for this author inPubMed Google Scholar RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE


Martín, M., Turk, E., Lostao, M. _et al._ Defects in Na+/glucose cotransporter (SGLT1) trafficking and function cause glucose-galactose malabsorption. _Nat Genet_ 12, 216–220 (1996).


https://doi.org/10.1038/ng0296-216 Download citation * Received: 11 September 1995 * Accepted: 22 November 1995 * Issue Date: 01 February 1996 * DOI: https://doi.org/10.1038/ng0296-216 SHARE


THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to


clipboard Provided by the Springer Nature SharedIt content-sharing initiative