Helicobacter pylori moves through mucus by reducing mucin viscoelasticity
The ulcer-causing gastric pathogen Helicobacter pylori is the only bacterium known to colonize the harsh acidic environment of the human stomach. H. pylori survives in acidic conditions by producing urease, which catalyzes hydrolysis of urea to yield ammonia thus elevating the pH of its environment....
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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United States National Academy of Sciences
2010
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| Online Access: | http://hdl.handle.net/1721.1/55287 https://orcid.org/0000-0003-4698-6488 |
| _version_ | 1826193637553209344 |
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| author | So, Peter T. C. Bansil, Rama Erramilli, Shyamsunder McKinley, Gareth H. Ewoldt, Randy H. Kelly, Ciaran P. Ghiran, Ionita Keates, Sarah Afdhal, Nezam H. Turner, Bradley S. Celli, Jonathan P. |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering So, Peter T. C. Bansil, Rama Erramilli, Shyamsunder McKinley, Gareth H. Ewoldt, Randy H. Kelly, Ciaran P. Ghiran, Ionita Keates, Sarah Afdhal, Nezam H. Turner, Bradley S. Celli, Jonathan P. |
| author_sort | So, Peter T. C. |
| collection | MIT |
| description | The ulcer-causing gastric pathogen Helicobacter pylori is the only bacterium known to colonize the harsh acidic environment of the human stomach. H. pylori survives in acidic conditions by producing urease, which catalyzes hydrolysis of urea to yield ammonia thus elevating the pH of its environment. However, the manner in which H. pylori is able to swim through the viscoelastic mucus gel that coats the stomach wall remains poorly understood. Previous rheology studies on gastric mucin, the key viscoelastic component of gastric mucus, indicate that the rheology of this material is pH dependent, transitioning from a viscous solution at neutral pH to a gel in acidic conditions. Bulk rheology measurements on porcine gastric mucin (PGM) show that pH elevation by H. pylori induces a dramatic decrease in viscoelastic moduli. Microscopy studies of the motility of H. pylori in gastric mucin at acidic and neutral pH in the absence of urea show that the bacteria swim freely at high pH, and are strongly constrained at low pH. By using two-photon fluorescence microscopy to image the bacterial motility in an initially low pH mucin gel with urea present we show that the gain of translational motility by bacteria is directly correlated with a rise in pH indicated by 2′,7′-Bis-(2-Carboxyethyl)-5-(and-6)-carboxyfluorescein (BCECF), a pH sensitive fluorescent dye. This study indicates that the helicoidal-shaped H. pylori does not bore its way through the mucus gel like a screw through a cork as has previously been suggested, but instead achieves motility by altering the rheological properties of its environment. |
| first_indexed | 2024-09-23T09:42:17Z |
| format | Article |
| id | mit-1721.1/55287 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T09:42:17Z |
| publishDate | 2010 |
| publisher | United States National Academy of Sciences |
| record_format | dspace |
| spelling | mit-1721.1/552872022-09-26T13:14:39Z Helicobacter pylori moves through mucus by reducing mucin viscoelasticity So, Peter T. C. Bansil, Rama Erramilli, Shyamsunder McKinley, Gareth H. Ewoldt, Randy H. Kelly, Ciaran P. Ghiran, Ionita Keates, Sarah Afdhal, Nezam H. Turner, Bradley S. Celli, Jonathan P. Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Mechanical Engineering Massachusetts Institute of Technology. Hatsopoulos Microfluids Laboratory So, Peter T. C. So, Peter T. C. The ulcer-causing gastric pathogen Helicobacter pylori is the only bacterium known to colonize the harsh acidic environment of the human stomach. H. pylori survives in acidic conditions by producing urease, which catalyzes hydrolysis of urea to yield ammonia thus elevating the pH of its environment. However, the manner in which H. pylori is able to swim through the viscoelastic mucus gel that coats the stomach wall remains poorly understood. Previous rheology studies on gastric mucin, the key viscoelastic component of gastric mucus, indicate that the rheology of this material is pH dependent, transitioning from a viscous solution at neutral pH to a gel in acidic conditions. Bulk rheology measurements on porcine gastric mucin (PGM) show that pH elevation by H. pylori induces a dramatic decrease in viscoelastic moduli. Microscopy studies of the motility of H. pylori in gastric mucin at acidic and neutral pH in the absence of urea show that the bacteria swim freely at high pH, and are strongly constrained at low pH. By using two-photon fluorescence microscopy to image the bacterial motility in an initially low pH mucin gel with urea present we show that the gain of translational motility by bacteria is directly correlated with a rise in pH indicated by 2′,7′-Bis-(2-Carboxyethyl)-5-(and-6)-carboxyfluorescein (BCECF), a pH sensitive fluorescent dye. This study indicates that the helicoidal-shaped H. pylori does not bore its way through the mucus gel like a screw through a cork as has previously been suggested, but instead achieves motility by altering the rheological properties of its environment. American Gastroenterological Association (Foundation for Digestive Health and Nutrition TAP Endowed Designated Research Award in Acid Related Diseases) 2010-05-26T14:50:57Z 2010-05-26T14:50:57Z 2009-08 Article http://purl.org/eprint/type/JournalArticle 1091-6490 0027-8424 http://hdl.handle.net/1721.1/55287 Celli, Jonathan P et al. “Helicobacter pylori moves through mucus by reducing mucin viscoelasticity.” Proceedings of the National Academy of Sciences 106.34 (2009): 14321-14326. © 2009 National Academy of Sciences https://orcid.org/0000-0003-4698-6488 en_US http://dx.doi.org/10.1073/pnas.0903438106 Proceedings of the National Academy of Sciences of the United States of America Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf United States National Academy of Sciences PNAS |
| spellingShingle | So, Peter T. C. Bansil, Rama Erramilli, Shyamsunder McKinley, Gareth H. Ewoldt, Randy H. Kelly, Ciaran P. Ghiran, Ionita Keates, Sarah Afdhal, Nezam H. Turner, Bradley S. Celli, Jonathan P. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity |
| title | Helicobacter pylori moves through mucus by reducing mucin viscoelasticity |
| title_full | Helicobacter pylori moves through mucus by reducing mucin viscoelasticity |
| title_fullStr | Helicobacter pylori moves through mucus by reducing mucin viscoelasticity |
| title_full_unstemmed | Helicobacter pylori moves through mucus by reducing mucin viscoelasticity |
| title_short | Helicobacter pylori moves through mucus by reducing mucin viscoelasticity |
| title_sort | helicobacter pylori moves through mucus by reducing mucin viscoelasticity |
| url | http://hdl.handle.net/1721.1/55287 https://orcid.org/0000-0003-4698-6488 |
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