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PMID: 10903344 Published · ppublish English Case Reports Journal Article Research Support, Non-U.S. Gov't

Congenital sucrase-isomaltase deficiency arising from cleavage and secretion of a mutant form of the enzyme.

The Journal of clinical investigation ·Vol. 106 ·No. 2 ·2000-07-00 ·Pages 281-7

Jacob R, Zimmer KP, Schmitz J, Naim HY

Abstract

Congenital sucrase-isomaltase deficiency (CSID) is an autosomal recessive human intestinal disorder that is clinically characterized by fermentative diarrhea, abdominal pain, and cramps upon ingestion of sugar. The symptoms are the consequence of absent or drastically reduced enzymatic activities of sucrase and isomaltase, the components of the intestinal integral membrane glycoprotein sucrase-isomaltase (SI). Several known phenotypes of CSID result from an altered posttranslational processing of SI. We describe here a novel CSID phenotype, in which pro-SI undergoes an unusual intracellular cleavage that eliminates its transmembrane domain. Biosynthesis of pro-SI in intestinal explants and in cells transfected with the SI cDNA of this phenotype demonstrated a cleavage occurring within the endoplasmic reticulum due to a point mutation that converts a leucine to proline at residue 340 of isomaltase. Cleaved pro-SI is transported to and processed in the Golgi apparatus and is ultimately secreted into the exterior milieu as an active enzyme. To our knowledge this is the first report of a disorder whose pathogenesis results not from protein malfolding or mistargeting, but from the conversion of an integral membrane glycoprotein into a secreted species that is lost from the cell surface.

MeSH Terms
Biological Transport Biopsy Carbohydrate Metabolism, Inborn Errors/genetics Cell Compartmentation Child, Preschool Golgi Apparatus/metabolism Humans Intestine, Small/ultrastructure Membrane Proteins/genetics Models, Molecular Phenotype Point Mutation Protein Precursors/metabolism Protein Processing, Post-Translational Sucrase-Isomaltase Complex/deficiency,genetics,metabolism
Chemicals
Membrane Proteins Protein Precursors Sucrase-Isomaltase Complex
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Jacob R
Department of Physiological Chemistry, School of Veterinary Medicine Hannover, Hannover, Germany.
Zimmer K P
Schmitz J
Naim H Y
References (31)
31 references, click to expand
  1. Structural determinants required for apical sorting of an intestinal brush-border membrane protein.
    J Biol Chem. 2000 Mar 3;275(9):6566-72 PMID: 10692463
  2. Positional preference of proline in alpha-helices.
    Protein Sci. 1999 Jul;8(7):1492-9 PMID: 10422838
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Biogenesis of intestinal plasma membrane: posttranslational route and cleavage of sucrase-isomaltase.
    Proc Natl Acad Sci U S A. 1979 Oct;76(10):5183-6 PMID: 291933
  5. Transport to cell surface of intestinal sucrase-isomaltase is blocked in the Golgi apparatus in a patient with congenital sucrase-isomaltase deficiency.
    Proc Natl Acad Sci U S A. 1985 Jul;82(13):4423-7 PMID: 3925457
  6. Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells.
    J Cell Biol. 1985 Sep;101(3):838-51 PMID: 3897250
  7. The sucrase-isomaltase complex: primary structure, membrane-orientation, and evolution of a stalked, intrinsic brush border protein.
    Cell. 1986 Jul 18;46(2):227-34 PMID: 3755079
  8. A study of the molecular pathology of sucrase-isomaltase deficiency. A defect in the intracellular processing of the enzyme.
    N Engl J Med. 1987 Feb 19;316(8):438-42 PMID: 3807985
  9. The posttranslational processing of sucrase-isomaltase in HT-29 cells is a function of their state of enterocytic differentiation.
    J Cell Biol. 1987 May;104(5):1199-205 PMID: 3553207
  10. Biosynthesis and maturation of lactase-phlorizin hydrolase in the human small intestinal epithelial cells.
    Biochem J. 1987 Jan 15;241(2):427-34 PMID: 3109375
  11. Identification of an endosomal antigen specific to absorptive cells of suckling rat ileum.
    J Cell Biol. 1987 Aug;105(2):691-703 PMID: 3305521
  12. Biosynthesis of the human sucrase-isomaltase complex. Differential O-glycosylation of the sucrase subunit correlates with its position within the enzyme complex.
    J Biol Chem. 1988 May 25;263(15):7242-53 PMID: 3366777
  13. Sucrase-isomaltase deficiency in humans. Different mutations disrupt intracellular transport, processing, and function of an intestinal brush border enzyme.
    J Clin Invest. 1988 Aug;82(2):667-79 PMID: 3403721
  14. Sequences beyond the cleavage site influence signal peptide function.
    J Biol Chem. 1988 Oct 25;263(30):15791-8 PMID: 3170612
  15. Mutations in signal sequence cleavage domain of preproparathyroid hormone alter protein translocation, signal sequence cleavage, and membrane-binding properties.
    Mol Endocrinol. 1989 Feb;3(2):240-50 PMID: 2710131
  16. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis.
    Cell. 1990 Nov 16;63(4):827-34 PMID: 1699669
  17. Expression of a full-length cDNA coding for human intestinal lactase-phlorizin hydrolase reveals an uncleaved, enzymatically active, and transport-competent protein.
    J Biol Chem. 1991 Jul 5;266(19):12313-20 PMID: 1905719
  18. Naturally occurring mutations in intestinal sucrase-isomaltase provide evidence for the existence of an intracellular sorting signal in the isomaltase subunit.
    J Cell Biol. 1991 Oct;115(1):45-57 PMID: 1717481
  19. Alteration of N-terminal residues of mature human lysozyme affects its secretion in yeast and translocation into canine microsomal vesicles.
    J Biol Chem. 1991 Oct 25;266(30):20363-8 PMID: 1939091
  20. Sequence of the complete cDNA and the 5' structure of the human sucrase-isomaltase gene. Possible homology with a yeast glucoamylase.
    Biochem J. 1992 Aug 1;285 ( Pt 3):915-23 PMID: 1353958
  21. Single amino acid substitutions can convert the uncleaved signal-anchor of sucrase-isomaltase to a cleaved signal sequence.
    J Biol Chem. 1992 Aug 25;267(24):16928-33 PMID: 1512234
  22. Transformation of the signal peptide/membrane anchor domain of a type II transmembrane protein into a cleavable signal peptide.
    J Biol Chem. 1993 Feb 5;268(4):2699-704 PMID: 8428944
  23. Deletion mutation in the signal anchor domain activates cleavage of the influenza virus neuraminidase, a type II transmembrane protein.
    J Gen Virol. 1994 May;75 ( Pt 5):1015-22 PMID: 8176363
  24. Ultrastructural, immunocytochemical and stereological investigation of hepatocytes in a patient with the mutation of the ornithine transcarbamylase gene.
    Eur J Cell Biol. 1995 May;67(1):73-83 PMID: 7641731
  25. Congenital sucrase-isomaltase deficiency. Identification of a glutamine to proline substitution that leads to a transport block of sucrase-isomaltase in a pre-Golgi compartment.
    J Clin Invest. 1996 Feb 1;97(3):633-41 PMID: 8609217
  26. A mutation in a highly conserved region in brush-border sucrase-isomaltase and lysosomal alpha-glucosidase results in Golgi retention.
    J Cell Sci. 1997 Mar;110 ( Pt 5):557-67 PMID: 9092938
  27. Compound missense mutations in the sodium/D-glucose cotransporter result in trafficking defects.
    Gastroenterology. 1997 Apr;112(4):1206-12 PMID: 9098004
  28. Mutation at the processing site of chicken low density lipoprotein receptor-related protein impairs efficient endoplasmic reticulum exit, but proteolytic cleavage is not essential for its endocytic functions.
    J Biol Chem. 1998 Oct 23;273(43):27779-85 PMID: 9774386
  29. Hierarchy of sorting signals in chimeras of intestinal lactase-phlorizin hydrolase and the influenza virus hemagglutinin.
    J Biol Chem. 1999 Mar 19;274(12):8061-7 PMID: 10075706
  30. O-linked glycans mediate apical sorting of human intestinal sucrase-isomaltase through association with lipid rafts.
    Curr Biol. 1999 Jun 3;9(11):593-6 PMID: 10359703
  31. Assay of intestinal disaccharidases.
    Anal Biochem. 1968 Jan;22(1):99-107 PMID: 5636962
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2000-07-00
Pages
281-7
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC314311
Subset
IM
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