Abstract
The pH within individual organelles of the secretory pathway is believed to be an important determinant of their biosynthetic activity. However, little is known about the determinants and regulation of the pH in the secretory organelles, which cannot be readily accessed by [H+]-sensitive probes. We devised a procedure for the dynamic, noninvasive measurement of pH in the lumen of the endoplasmic reticulum in intact mammalian cells. A recombinant form of the B subunit of Shiga toxin, previously modified to include a carboxyl-terminal KDEL sequence and a pH-sensitive fluorophore, was used for a two-stage delivery strategy. Retrograde traffic of endogenous lipids was harnessed to target this protein to the Golgi complex, followed by retrieval to the endoplasmic reticulum (ER) by KDEL receptors. Immunofluorescence and immunoelectron microscopy were used to verify the subcellular localization of the modified B fragment. Fluorescence ratio imaging and two independent calibration procedures were applied to determine the pH of the ER in situ. We found that the pH of the endoplasmic reticulum is near neutral and is unaffected during agonist-induced release of calcium. The ER was found to be highly permeable to H+ (equivalents), so that the prevailing [H+] is susceptible to alterations in the cytosolic pH. Plasmalemmal acid-base transporters were shown to indirectly regulate the endoplasmic reticulum pH.
MeSH Terms
Bacterial Toxins
Biological Transport
Calcium/metabolism
Endoplasmic Reticulum/physiology
Fluoresceins
Fluorescent Antibody Technique
Fluorescent Dyes
HeLa Cells
Humans
Hydrogen-Ion Concentration
Microscopy, Immunoelectron/methods
Oligopeptides
Protein Sorting Signals
Shiga Toxins
Chemicals
Bacterial Toxins
Fluoresceins
Fluorescent Dyes
Oligopeptides
Protein Sorting Signals
Shiga Toxins
lysyl-aspartyl-glutamyl-leucine
5-((4,6-dichloro-1,3,5-triazin-2-yl)amino)fluorescein
2',7'-bis(carboxyethyl)-5(6)-carboxyfluorescein
Calcium
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Kim J H
Division of Gastroenterology and Nutrition, Research Institute, Hospital for Sick Children, 555 University Avenue, Toronto, ON, Canada M5G 1X8.
Johannes L
Goud B
Antony C
Lingwood C A
Daneman R
Grinstein S
References (19)
19 references, click to expand
-
Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ.
Biochemistry. 1979 May 29;18(11):2210-8
PMID: 36128
-
Na+/H+ exchangers of mammalian cells.
J Biol Chem. 1997 Sep 5;272(36):22373-6
PMID: 9278382
-
Metabolic regulation via intracellular pH.
Am J Physiol. 1984 Apr;246(4 Pt 2):R409-38
PMID: 6326601
-
New method for calculating pHi from accurately measured changes in pHi induced by a weak acid and base.
Pflugers Arch. 1986 Jul;407(1):59-63
PMID: 3737383
-
Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles.
J Cell Biol. 1986 Dec;103(6 Pt 1):2273-81
PMID: 3536964
-
Competitive, reversible, and potent antagonism of inositol 1,4,5-trisphosphate-activated calcium release by heparin.
J Biol Chem. 1988 Aug 15;263(23):11075-9
PMID: 3136153
-
A novel method for absolute calibration of intracellular pH indicators.
Pflugers Arch. 1989 Mar;413(5):553-8
PMID: 2740208
-
Histamine-H1-receptor-mediated phosphoinositide hydrolysis, Ca2+ signalling and membrane-potential oscillations in human HeLa carcinoma cells.
Biochem J. 1990 Feb 15;266(1):235-43
PMID: 2155607
-
Recycling of proteins from the Golgi compartment to the ER in yeast.
J Cell Biol. 1990 Aug;111(2):369-77
PMID: 2199456
-
Characterization of Shiga-like toxin I B subunit purified from overproducing clones of the SLT-I B cistron.
Biochem J. 1990 Dec 15;272(3):805-11
PMID: 2268304
-
Construction of stable LamB-Shiga toxin B subunit hybrids: analysis of expression in Salmonella typhimurium aroA strains and stimulation of B subunit-specific mucosal and serum antibody responses.
Infect Immun. 1992 Aug;60(8):3345-59
PMID: 1639503
-
Local conformational change in the B-subunit of Shiga-like toxin 1 at endosomal pH.
Biochemistry. 1993 Jan 26;32(3):918-22
PMID: 8380713
-
Universal method for the facile production of glycolipid/lipid matrices for the affinity purification of binding ligands.
Anal Biochem. 1994 Feb 15;217(1):1-6
PMID: 8203724
-
Rapid heparin-sensitive Ca2+ release following Ca(2+)-ATPase inhibition in intact HL-60 granulocytes. Evidence for Ins(1,4,5)P3-dependent Ca2+ cycling across the membrane of Ca2+ stores.
Biochem J. 1994 Aug 15;302 ( Pt 1):155-62
PMID: 8068001
-
The thapsigargin-evoked increase in [Ca2+]i involves an InsP3-dependent Ca2+ release process in pancreatic acinar cells.
Pflugers Arch. 1994 Jun;427(3-4):325-31
PMID: 8072853
-
Dynamic measurement of the pH of the Golgi complex in living cells using retrograde transport of the verotoxin receptor.
J Cell Biol. 1996 Sep;134(6):1387-99
PMID: 8830769
-
Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin.
Physiol Rev. 1996 Oct;76(4):949-66
PMID: 8874490
-
Retrograde transport of KDEL-bearing B-fragment of Shiga toxin.
J Biol Chem. 1997 Aug 1;272(31):19554-61
PMID: 9235960
-
Golgi membranes contain an electrogenic H+ pump in parallel to a chloride conductance.
J Cell Biol. 1983 Oct;97(4):1303-8
PMID: 6225785