Author:
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-
1.
Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB, 2012. Cholera. Lancet 379: 2466–2476.
-
2.
Fleckenstein JM, Hardwidge PR, Munson GP, Rasko DA, Sommerfelt H, Steinsland H, 2010. Molecular mechanisms of enterotoxigenic Escherichia coli infection. Microbes Infect 12: 89–98.
-
3.
Kopic S, Geibel JP, 2010. Toxin mediated diarrhea in the 21 century: the pathophysiology of intestinal ion transport in the course of ETEC, V. cholerae and rotavirus infection. Toxins (Basel) 2: 2132–2157.
-
4.
Anstee DJ, 2010. The relationship between blood groups and disease. Blood 115: 4635–4643.
-
5.
Boren T, Falk P, Roth KA, Larson G, Normark S, 1993. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262: 1892–1895.
-
6.
Glass RI, Holmgren J, Haley CE, Khan MR, Svennerholm AM, Stoll BJ, Belayet Hossain KM, Black RE, Yunus M, Barua D, 1985. Predisposition for cholera of individuals with O blood group. Possible evolutionary significance. Am J Epidemiol 121: 791–796.
-
7.
Harris JB, Khan AI, LaRocque RC, Dorer DJ, Chowdhury F, Faruque AS, Sack DA, Ryan ET, Qadri F, Calderwood SB, 2005. Blood group, immunity, and risk of infection with Vibrio cholerae in an area of endemicity. Infect Immun 73: 7422–7427.
-
8.
Karlsson EK, Harris JB, Tabrizi S, Rahman A, Shlyakhter I, Patterson N, O'Dushlaine C, Schaffner SF, Gupta S, Chowdhury F, Sheikh A, Shin OS, Ellis C, Becker CE, Stuart LM, Calderwood SB, Ryan ET, Qadri F, Sabeti PC, Larocque RC, 2013. Natural selection in a Bangladeshi population from the cholera-endemic Ganges River Delta. Sci Transl Med 5: 192ra86.
-
9.
Heggelund JE, Haugen E, Lygren B, Mackenzie A, Holmner A, Vasile F, Reina JJ, Bernardi A, Krengel U, 2012. Both El Tor and classical cholera toxin bind blood group determinants. Biochem Biophys Res Commun 418: 731–735.
-
10.
Holmner A, Mackenzie A, Krengel U, 2010. Molecular basis of cholera blood-group dependence and implications for a world characterized by climate change. FEBS Lett 584: 2548–2555.
-
11.
Holmner A, Lebens M, Teneberg S, Angstrom J, Okvist M, Krengel U, 2004. Novel binding site identified in a hybrid between cholera toxin and heat-labile enterotoxin: 1.9 A crystal structure reveals the details. Structure 12: 1655–1667.
-
12.
Vasile F, Reina JJ, Potenza D, Heggelund JE, Mackenzie A, Krengel U, Bernardi A, 2014. Comprehensive analysis of blood group antigen binding to classical and El Tor cholera toxin B-pentamers by NMR. Glycobiology 24: 766–778.
-
13.
Cuatrecasas P, 1973. Gangliosides and membrane receptors for cholera toxin. Biochemistry 12: 3558–3566.
-
14.
Hansson HA, Holmgren J, Svennerholm L, 1977. Ultrastructural localization of cell membrane GM1 ganglioside by cholera toxin. Proc Natl Acad Sci USA 74: 3782–3786.
-
15.
VanDussen KL, Marinshaw JM, Shaikh N, Miyoshi H, Moon C, Tarr PI, Ciorba MA, Stappenbeck TS, 2015. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut 64: 911–920.
-
16.
Taki T, Kibayashi K, 2014. A simple ABO genotyping by PCR using sequence-specific primers with mismatched nucleotides. Leg Med (Tokyo) 16: 168–172.
-
17.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A, 2012. Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676–682.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2491 | 2197 | 82 |
| Full Text Views | 880 | 36 | 8 |
| PDF Downloads | 473 | 34 | 7 |
Blood Group O–Dependent Cellular Responses to Cholera Toxin: Parallel Clinical and Epidemiological Links to Severe Cholera
F. Matthew Kuhlmann
F. Matthew Kuhlmann
Division of Infectious Diseases, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, Missouri.
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Srikanth Santhanam
Srikanth Santhanam
Division of Gastroenterology, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, Missouri.
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Pardeep Kumar
Pardeep Kumar
Division of Infectious Diseases, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, Missouri.
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Qingwei Luo
Qingwei Luo
Division of Infectious Diseases, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, Missouri.
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Matthew A. Ciorba
Matthew A. Ciorba
Division of Gastroenterology, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, Missouri.
Molecular Microbiology and Microbial Pathogenesis Program, Division of Biology and Biomedical Sciences, Washington University School of Medicine, Saint Louis, Missouri.
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James M. Fleckenstein
James M. Fleckenstein
Division of Infectious Diseases, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, Missouri.
Molecular Microbiology and Microbial Pathogenesis Program, Division of Biology and Biomedical Sciences, Washington University School of Medicine, Saint Louis, Missouri.
Veterans Affairs Medical Center, Saint Louis, Missouri.
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Because O blood group has been associated with more severe cholera infections, it has been hypothesized that cholera toxin (CT) may bind non-O blood group antigens of the intestinal mucosae, thereby preventing efficient interaction with target GM1 gangliosides required for uptake of the toxin and activation of cyclic adenosine monophosphate (cAMP) signaling in target epithelia. Herein, we show that after exposure to CT, human enteroids expressing O blood group exhibited marked increase in cAMP relative to cells derived from blood group A individuals. Likewise, using CRISPR/Cas9 engineering, a functional group O line (HT-29-A−/−) was generated from a parent group A HT-29 line. CT stimulated robust cAMP responses in HT-29-A−/− cells relative to HT-29 cells. These findings provide a direct molecular link between blood group O expression and differential cellular responses to CT, recapitulating clinical and epidemiologic observations.
Author Notes
Financial support: This work was supported by funding from the Department of Veterans Affairs(grant 5I01BX001469); grant R01AI89894 from the National Institutes of Health, National Institute of Allergy and Infectious Diseases (NIAID); CTSA grant UL1 TR000448 from the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health (NIH), and the Digestive Diseases Research Core Center at Washington University School of Medicine; grant P30 DK52574 from the National Institute of Diabetes and Digestive and Kidney Diseases. Matthew A. Ciorba was supported by grants DK100737, DK089016, and DK109384 from the NIDDK, AI095776 from the NIAID, and a Crohn's and Colitis Foundation Senior Research Award.
Authors' addresses: F. Matthew Kuhlmann, Pardeep Kumar, and Qingwei Luo, Division of Infectious Diseases, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, MO, E-mails: fkuhlman@dom.wustl.edu, pradeepkumar.19@gmail.com, and qluo@dom.wustl.edu. Srikanth Santhanam, Division of Gastroenterology, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, MO, E-mail: ssanthan@dom.wustl.edu. Matthew A. Ciorba, Division of Gastroenterology, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, MO, and Molecular Microbiology and Microbial Pathogenesis Program, Division of Biology and Biomedical Sciences, Washington University School of Medicine, Saint Louis, MO, E-mail: mciorba@dom.wustl.edu. James M. Fleckenstein, Division of Infectious Diseases, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, MO, John Cochran Division, Veterans Affairs Medical Center, Saint Louis, MO, and Molecular Microbiology and Microbial Pathogenesis Program, Division of Biology and Biomedical Sciences, Washington University School of Medicine, Saint Louis, MO, E-mail: jflecken@dom.wustl.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB, 2012. Cholera. Lancet 379: 2466–2476.
-
2.
Fleckenstein JM, Hardwidge PR, Munson GP, Rasko DA, Sommerfelt H, Steinsland H, 2010. Molecular mechanisms of enterotoxigenic Escherichia coli infection. Microbes Infect 12: 89–98.
-
3.
Kopic S, Geibel JP, 2010. Toxin mediated diarrhea in the 21 century: the pathophysiology of intestinal ion transport in the course of ETEC, V. cholerae and rotavirus infection. Toxins (Basel) 2: 2132–2157.
-
4.
Anstee DJ, 2010. The relationship between blood groups and disease. Blood 115: 4635–4643.
-
5.
Boren T, Falk P, Roth KA, Larson G, Normark S, 1993. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262: 1892–1895.
-
6.
Glass RI, Holmgren J, Haley CE, Khan MR, Svennerholm AM, Stoll BJ, Belayet Hossain KM, Black RE, Yunus M, Barua D, 1985. Predisposition for cholera of individuals with O blood group. Possible evolutionary significance. Am J Epidemiol 121: 791–796.
-
7.
Harris JB, Khan AI, LaRocque RC, Dorer DJ, Chowdhury F, Faruque AS, Sack DA, Ryan ET, Qadri F, Calderwood SB, 2005. Blood group, immunity, and risk of infection with Vibrio cholerae in an area of endemicity. Infect Immun 73: 7422–7427.
-
8.
Karlsson EK, Harris JB, Tabrizi S, Rahman A, Shlyakhter I, Patterson N, O'Dushlaine C, Schaffner SF, Gupta S, Chowdhury F, Sheikh A, Shin OS, Ellis C, Becker CE, Stuart LM, Calderwood SB, Ryan ET, Qadri F, Sabeti PC, Larocque RC, 2013. Natural selection in a Bangladeshi population from the cholera-endemic Ganges River Delta. Sci Transl Med 5: 192ra86.
-
9.
Heggelund JE, Haugen E, Lygren B, Mackenzie A, Holmner A, Vasile F, Reina JJ, Bernardi A, Krengel U, 2012. Both El Tor and classical cholera toxin bind blood group determinants. Biochem Biophys Res Commun 418: 731–735.
-
10.
Holmner A, Mackenzie A, Krengel U, 2010. Molecular basis of cholera blood-group dependence and implications for a world characterized by climate change. FEBS Lett 584: 2548–2555.
-
11.
Holmner A, Lebens M, Teneberg S, Angstrom J, Okvist M, Krengel U, 2004. Novel binding site identified in a hybrid between cholera toxin and heat-labile enterotoxin: 1.9 A crystal structure reveals the details. Structure 12: 1655–1667.
-
12.
Vasile F, Reina JJ, Potenza D, Heggelund JE, Mackenzie A, Krengel U, Bernardi A, 2014. Comprehensive analysis of blood group antigen binding to classical and El Tor cholera toxin B-pentamers by NMR. Glycobiology 24: 766–778.
-
13.
Cuatrecasas P, 1973. Gangliosides and membrane receptors for cholera toxin. Biochemistry 12: 3558–3566.
-
14.
Hansson HA, Holmgren J, Svennerholm L, 1977. Ultrastructural localization of cell membrane GM1 ganglioside by cholera toxin. Proc Natl Acad Sci USA 74: 3782–3786.
-
15.
VanDussen KL, Marinshaw JM, Shaikh N, Miyoshi H, Moon C, Tarr PI, Ciorba MA, Stappenbeck TS, 2015. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut 64: 911–920.
-
16.
Taki T, Kibayashi K, 2014. A simple ABO genotyping by PCR using sequence-specific primers with mismatched nucleotides. Leg Med (Tokyo) 16: 168–172.
-
17.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A, 2012. Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676–682.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2491 | 2197 | 82 |
| Full Text Views | 880 | 36 | 8 |
| PDF Downloads | 473 | 34 | 7 |