1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

A Cinematic View of Tissue Microbiology in the Live Infected Host

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Agneta Richter-Dahlfors1, Keira Melican2
  • Editors: Pascale Cossart3, Craig R. Roy4, Philippe Sansonetti5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Swedish Medical Nanoscience Centre, Department of Neuroscience, Karolinska Institutet, SE-17177, Stockholm, Sweden; 2: Swedish Medical Nanoscience Centre, Department of Neuroscience, Karolinska Institutet, SE-17177, Stockholm, Sweden; 3: Institut Pasteur, Paris, France; 4: Yale University School of Medicine, New Haven, Connecticut; 5: Institut Pasteur, Paris, France
  • Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.BAI-0007-2019
  • Received 06 April 2018 Accepted 15 February 2019 Published 31 May 2019
  • Agneta Richter-Dahlfors, [email protected]; Keira Melican, [email protected]
image of A Cinematic View of Tissue Microbiology in the Live Infected Host
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    A Cinematic View of Tissue Microbiology in the Live Infected Host, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/7/3/BAI-0007-2019-1.gif /docserver/preview/fulltext/microbiolspec/7/3/BAI-0007-2019-2.gif
  • Abstract:

    Tissue microbiology allows for the study of bacterial infection in the most clinically relevant microenvironment, the living host. Advancements in techniques and technology have facilitated the development of novel ways of studying infection. Many of these advancements have come from outside the field of microbiology. In this article, we outline the progression from bacteriology through cellular microbiology to tissue microbiology, highlighting seminal studies along the way. We outline the enormous potential but also some of the challenges of the tissue microbiology approach. We focus on the role of emerging technologies in the continual development of infectious disease research and highlight future possibilities in our ongoing quest to understand host-pathogen interaction.

  • Citation: Richter-Dahlfors A, Melican K. 2019. A Cinematic View of Tissue Microbiology in the Live Infected Host. Microbiol Spectrum 7(3):BAI-0007-2019. doi:10.1128/microbiolspec.BAI-0007-2019.

References

1. Hazelwood KL, Olenych SG, Griffin JD, Cathcart JA, Davidson MW. 2007. Entering the portal: understanding the digital image recorded through a microscope, p 3–43. In Shorte SL, Frischknecht F (ed), Imaging Cellular and Molecular Biological Functions. Springer, Heidelberg, Germany. http://dx.doi.org/10.1007/978-3-540-71331-9_1.
2. Ruestow EG. 1996. The Microscope in the Dutch Republic. Cambridge University Press, New York, NY.
3. Mims C, Dockrell HM, Goering RV, Roitt I, Wakelin D, Zuckerman M. 2004. Medical Microbiology, 3rd ed. Elsevier Mosby, London, United Kingdom.
4. Cossart P, Boquet P, Normark S, Rappuoli R. 1996. Cellular microbiology emerging. Science 271:315–316 http://dx.doi.org/10.1126/science.271.5247.315. [PubMed]
5. Anonymous. 2006. Infection biology. Nature 441:255–256 http://dx.doi.org/10.1038/441255b.
6. Richter Dahlfors AA, Kurland CG. 1990. Novel mutants of elongation factor G. J Mol Biol 215:549–557 http://dx.doi.org/10.1016/S0022-2836(05)80167-6.
7. Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vázquez A, Barba J, Ibarra JA, O’Donnell P, Metalnikov P, Ashman K, Lee S, Goode D, Pawson T, Finlay BB. 2004. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A 101:3597–3602 http://dx.doi.org/10.1073/pnas.0400326101. [PubMed]
8. Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, Dupuy C, Babinet C, Cossart P. 2001. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292:1722–1725 http://dx.doi.org/10.1126/science.1059852. [PubMed]
9. Richter-Dahlfors A, Buchan AM, Finlay BB. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186:569–580 http://dx.doi.org/10.1084/jem.186.4.569. [PubMed]
10. Tam VC, Serruto D, Dziejman M, Brieher W, Mekalanos JJ. 2007. A type III secretion system in Vibrio cholerae translocates a formin/spire hybrid-like actin nucleator to promote intestinal colonization. Cell Host Microbe 1:95–107 http://dx.doi.org/10.1016/j.chom.2007.03.005. [PubMed]
11. Chieppa M, Rescigno M, Huang AY, Germain RN. 2006. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med 203:2841–2852 http://dx.doi.org/10.1084/jem.20061884. [PubMed]
12. Han JJ, Kunde YA, Hong-Geller E, Werner JH. 2014. Actin restructuring during Salmonella typhimurium infection investigated by confocal and super-resolution microscopy. J Biomed Opt 19:016011 http://dx.doi.org/10.1117/1.JBO.19.1.016011. [PubMed]
13. Melican K, Richter-Dahlfors A. 2009. Real-time live imaging to study bacterial infections in vivo. Curr Opin Microbiol 12:31–36 http://dx.doi.org/10.1016/j.mib.2008.11.002. [PubMed]
14. Molitoris BA, Sandoval RM. 2009. Techniques to study nephron function: microscopy and imaging. Pflugers Arch 458:203–209 http://dx.doi.org/10.1007/s00424-008-0629-8. [PubMed]
15. Dunn KW, Sandoval RM, Molitoris BA. 2003. Intravital imaging of the kidney using multiparameter multiphoton microscopy. Nephron Exp Nephrol 94:e7–e11 http://dx.doi.org/10.1159/000070813. [PubMed]
16. Molitoris BA, Sandoval RM. 2005. Intravital multiphoton microscopy of dynamic renal processes. Am J Physiol Renal Physiol 288:F1084–F1089 http://dx.doi.org/10.1152/ajprenal.00473.2004. [PubMed]
17. Månsson LE, Melican K, Boekel J, Sandoval RM, Hautefort I, Tanner GA, Molitoris BA, Richter-Dahlfors A. 2007. Real-time studies of the progression of bacterial infections and immediate tissue responses in live animals. Cell Microbiol 9:413–424 http://dx.doi.org/10.1111/j.1462-5822.2006.00799.x. [PubMed]
18. Melican K, Boekel J, Månsson LE, Sandoval RM, Tanner GA, Källskog O, Palm F, Molitoris BA, Richter-Dahlfors A. 2008. Bacterial infection-mediated mucosal signalling induces local renal ischaemia as a defence against sepsis. Cell Microbiol 10:1987–1998 http://dx.doi.org/10.1111/j.1462-5822.2008.01182.x. [PubMed]
19. Melican K, Sandoval RM, Kader A, Josefsson L, Tanner GA, Molitoris BA, Richter-Dahlfors A. 2011. Uropathogenic Escherichia coli P and type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction. PLoS Pathog 7:e1001298 http://dx.doi.org/10.1371/journal.ppat.1001298. [PubMed]
20. Farache J, Koren I, Milo I, Gurevich I, Kim KW, Zigmond E, Furtado GC, Lira SA, Shakhar G. 2013. Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 38:581–595 http://dx.doi.org/10.1016/j.immuni.2013.01.009. [PubMed]
21. Abtin A, Jain R, Mitchell AJ, Roediger B, Brzoska AJ, Tikoo S, Cheng Q, Ng LG, Cavanagh LL, von Andrian UH, Hickey MJ, Firth N, Weninger W. 2014. Perivascular macrophages mediate neutrophil recruitment during bacterial skin infection. Nat Immunol 15:45–53 http://dx.doi.org/10.1038/ni.2769. [PubMed]
22. Fiole D, Deman P, Trescos Y, Mayol JF, Mathieu J, Vial JC, Douady J, Tournier JN. 2014. Two-photon intravital imaging of lungs during anthrax infection reveals long-lasting macrophage-dendritic cell contacts. Infect Immun 82:864–872 http://dx.doi.org/10.1128/IAI.01184-13. [PubMed]
23. Schulz A, Chuquimia OD, Antypas H, Steiner SE, Sandoval RM, Tanner GA, Molitoris BA, Richter-Dahlfors A, Melican K. 2018. Protective vascular coagulation in response to bacterial infection of the kidney is regulated by bacterial lipid A and host CD147. Pathog Dis 76: http://dx.doi.org/10.1093/femspd/fty087. [PubMed]
24. Sutton TA, Mang HE, Campos SB, Sandoval RM, Yoder MC, Molitoris BA. 2003. Injury of the renal microvascular endothelium alters barrier function after ischemia. Am J Physiol Renal Physiol 285:F191–F198 http://dx.doi.org/10.1152/ajprenal.00042.2003. [PubMed]
25. Molitoris BA, Sutton TA. 2004. Endothelial injury and dysfunction: role in the extension phase of acute renal failure. Kidney Int 66:496–499 http://dx.doi.org/10.1111/j.1523-1755.2004.761_5.x. [PubMed]
26. Schaffer K, Taylor CT. 2015. The impact of hypoxia on bacterial infection. FEBS J 282:2260–2266 http://dx.doi.org/10.1111/febs.13270. [PubMed]
27. Jennewein J, Matuszak J, Walter S, Felmy B, Gendera K, Schatz V, Nowottny M, Liebsch G, Hensel M, Hardt WD, Gerlach RG, Jantsch J. 2015. Low-oxygen tensions found in Salmonella-infected gut tissue boost Salmonella replication in macrophages by impairing antimicrobial activity and augmenting Salmonella virulence. Cell Microbiol 17:1833–1847 http://dx.doi.org/10.1111/cmi.12476. [PubMed]
28. Marteyn B, West NP, Browning DF, Cole JA, Shaw JG, Palm F, Mounier J, Prévost MC, Sansonetti P, Tang CM. 2010. Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465:355–358 http://dx.doi.org/10.1038/nature08970. [PubMed]
29. Wilde AD, Snyder DJ, Putnam NE, Valentino MD, Hammer ND, Lonergan ZR, Hinger SA, Aysanoa EE, Blanchard C, Dunman PM, Wasserman GA, Chen J, Shopsin B, Gilmore MS, Skaar EP, Cassat JE. 2015. Bacterial hypoxic responses revealed as critical determinants of the host-pathogen outcome by TnSeq analysis of Staphylococcus aureus invasive infection. PLoS Pathog 11:e1005341 http://dx.doi.org/10.1371/journal.ppat.1005341. [PubMed]
30. Monceaux V, Chiche-Lapierre C, Chaput C, Witko-Sarsat V, Prevost MC, Taylor CT, Ungeheuer MN, Sansonetti PJ, Marteyn BS. 2016. Anoxia and glucose supplementation preserve neutrophil viability and function. Blood 128:993–1002 http://dx.doi.org/10.1182/blood-2015-11-680918. [PubMed]
31. Egners A, Erdem M, Cramer T. 2016. The response of macrophages and neutrophils to hypoxia in the context of cancer and other inflammatory diseases. Mediators Inflamm 2016:2053646 http://dx.doi.org/10.1155/2016/2053646. [PubMed]
32. Roch-Ramel F, Peters G. 1979. Micropuncture techniques as a tool in renal pharmacology. Annu Rev Pharmacol Toxicol 19:323–345 http://dx.doi.org/10.1146/annurev.pa.19.040179.001543. [PubMed]
33. Surewaard BG, Deniset JF, Zemp FJ, Amrein M, Otto M, Conly J, Omri A, Yates RM, Kubes P. 2016. Identification and treatment of the Staphylococcus aureus reservoir in vivo. J Exp Med 213:1141–1151 http://dx.doi.org/10.1084/jem.20160334. (Erratum, 213:3087. doi:10.1084/jem.2016033411032016c.) [PubMed]
34. Kolaczkowska E, Jenne CN, Surewaard BG, Thanabalasuriar A, Lee WY, Sanz MJ, Mowen K, Opdenakker G, Kubes P. 2015. Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nat Commun 6:6673 http://dx.doi.org/10.1038/ncomms7673. [PubMed]
35. Kolesnikov M, Farache J, Shakhar G. 2015. Intravital two-photon imaging of the gastrointestinal tract. J Immunol Methods 421:73–80 http://dx.doi.org/10.1016/j.jim.2015.03.008. [PubMed]
36. Rodriguez-Tirado C, Kitamura T, Kato Y, Pollard JW, Condeelis JS, Entenberg D. 2016. Long-term high-resolution intravital microscopy in the lung with a vacuum stabilized imaging window. J Vis Exp (116) :e54603. http://dx.doi.org/10.3791/54603. [PubMed]
37. Looney MR, Thornton EE, Sen D, Lamm WJ, Glenny RW, Krummel MF. 2011. Stabilized imaging of immune surveillance in the mouse lung. Nat Methods 8:91–96 http://dx.doi.org/10.1038/nmeth.1543. [PubMed]
38. Leung C, Chijioke O, Gujer C, Chatterjee B, Antsiferova O, Landtwing V, McHugh D, Raykova A, Münz C. 2013. Infectious diseases in humanized mice. Eur J Immunol 43:2246–2254 http://dx.doi.org/10.1002/eji.201343815. [PubMed]
39. Rämer PC, Chijioke O, Meixlsperger S, Leung CS, Münz C. 2011. Mice with human immune system components as in vivo models for infections with human pathogens. Immunol Cell Biol 89:408–416 http://dx.doi.org/10.1038/icb.2010.151. [PubMed]
40. Soyer M, Charles-Orszag A, Lagache T, Machata S, Imhaus AF, Dumont A, Millien C, Olivo-Marin JC, Duménil G. 2014. Early sequence of events triggered by the interaction of Neisseria meningitidis with endothelial cells. Cell Microbiol 16:878–895 http://dx.doi.org/10.1111/cmi.12248. [PubMed]
41. Chamot-Rooke J, Mikaty G, Malosse C, Soyer M, Dumont A, Gault J, Imhaus AF, Martin P, Trellet M, Clary G, Chafey P, Camoin L, Nilges M, Nassif X, Duménil G. 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331:778–782 http://dx.doi.org/10.1126/science.1200729. [PubMed]
42. Mairey E, Genovesio A, Donnadieu E, Bernard C, Jaubert F, Pinard E, Seylaz J, Olivo-Marin JC, Nassif X, Duménil G. 2006. Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood-brain barrier. J Exp Med 203:1939–1950 http://dx.doi.org/10.1084/jem.20060482. [PubMed]
43. Melican K, Michea Veloso P, Martin T, Bruneval P, Duménil G. 2013. Adhesion of Neisseria meningitidis to dermal vessels leads to local vascular damage and purpura in a humanized mouse model. PLoS Pathog 9:e1003139 http://dx.doi.org/10.1371/journal.ppat.1003139. [PubMed]
44. Melican K, Duménil G. 2013. A humanized model of microvascular infection. Future Microbiol 8:567–569 http://dx.doi.org/10.2217/fmb.13.35. [PubMed]
45. Sjöqvist J, Maria J, Simon RA, Linares M, Norman P, Nilsson KPR, Lindgren M. 2014. Toward a molecular understanding of the detection of amyloid proteins with flexible conjugated oligothiophenes. J Phys Chem A 118:9820–9827 http://dx.doi.org/10.1021/jp506797j. [PubMed]
46. Klingstedt T, Aslund A, Simon RA, Johansson LB, Mason JJ, Nyström S, Hammarström P, Nilsson KP. 2011. Synthesis of a library of oligothiophenes and their utilization as fluorescent ligands for spectral assignment of protein aggregates. Org Biomol Chem 9:8356–8370 http://dx.doi.org/10.1039/c1ob05637a. [PubMed]
47. Smith DR, Price JE, Burby PE, Blanco LP, Chamberlain J, Chapman MR. 2017. The production of curli amyloid fibers is deeply integrated into the biology of Escherichia coli. Biomolecules 7:E75 http://dx.doi.org/10.3390/biom7040075. [PubMed]
48. Choong FX, Bäck M, Fahlén S, Johansson LB, Melican K, Rhen M, Nilsson KPR, Richter-Dahlfors A. 2016. Real-time optotracing of curli and cellulose in live Salmonella biofilms using luminescent oligothiophenes. NPJ Biofilms Microbiomes 2:16024 http://dx.doi.org/10.1038/npjbiofilms.2016.24. [PubMed]
49. Antypas H, Choong FX, Libberton B, Brauner A, Richter-Dahlfors A. 2018. Rapid diagnostic assay for detection of cellulose in urine as biomarker for biofilm-related urinary tract infections. NPJ Biofilms Microbiomes 4:26 http://dx.doi.org/10.1038/s41522-018-0069-y. [PubMed]
50. Komura D, Ishikawa S. 2018. Machine learning methods for histopathological image analysis. Comput Struct Biotechnol J 16:34–42 http://dx.doi.org/10.1016/j.csbj.2018.01.001. [PubMed]
51. Melendez J, van Ginneken B, Maduskar P, Philipsen RH, Ayles H, Sanchez CI. 2016. On combining multiple-instance learning and active learning for computer-aided detection of tuberculosis. IEEE Trans Med Imaging 35:1013–1024 http://dx.doi.org/10.1109/TMI.2015.2505672. [PubMed]
52. Löffler S, Melican K, Nilsson KPR, Richter-Dahlfors A. 2017. Organic bioelectronics in medicine. J Intern Med 282:24–36 http://dx.doi.org/10.1111/joim.12595. [PubMed]
53. Löffler S, Libberton B, Richter-Dahlfors A. 2015. Organic bioelectronic tools for biomedical applications. Electronics (Basel) 4:879–908 http://dx.doi.org/10.3390/electronics4040879.
54. Löffler S, Libberton B, Richter-Dahlfors A. 2015. Organic bioelectronics in infection. J Mater Chem B Mater Biol Med 3:4979–4992 http://dx.doi.org/10.1039/C5TB00382B.
55. Boekel J, Källskog O, Rydén-Aulin M, Rhen M, Richter-Dahlfors A. 2011. Comparative tissue transcriptomics reveal prompt inter-organ communication in response to local bacterial kidney infection. BMC Genomics 12:123 http://dx.doi.org/10.1186/1471-2164-12-123. [PubMed]
56. Goda T, Kjall P, Ishihara K, Richter-Dahlfors A, Miyahara Y. 2014. Biomimetic interfaces reveal activation dynamics of C-reactive protein in local microenvironments. Adv Healthc Mater 3:1733–1738 http://dx.doi.org/10.1002/adhm.201300625. [PubMed]
57. Isaksson J, Kjäll P, Nilsson D, Robinson ND, Berggren M, Richter-Dahlfors A. 2007. Electronic control of Ca2+ signalling in neuronal cells using an organic electronic ion pump. Nat Mater 6:673–679 http://dx.doi.org/10.1038/nmat1963. [PubMed]
58. Richter-Dahlfors A, Rhen M, Udekwu K. 2012. Tissue microbiology provides a coherent picture of infection. Curr Opin Microbiol 15:15–22 http://dx.doi.org/10.1016/j.mib.2011.10.009. [PubMed]
59. Stolp B, Melican K. 2016. Microbial pathogenesis revealed by intravital microscopy: pros, cons and cautions. FEBS Lett 590:2014–2026 http://dx.doi.org/10.1002/1873-3468.12122. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.BAI-0007-2019
2019-05-31
2019-06-16

Abstract:

Tissue microbiology allows for the study of bacterial infection in the most clinically relevant microenvironment, the living host. Advancements in techniques and technology have facilitated the development of novel ways of studying infection. Many of these advancements have come from outside the field of microbiology. In this article, we outline the progression from bacteriology through cellular microbiology to tissue microbiology, highlighting seminal studies along the way. We outline the enormous potential but also some of the challenges of the tissue microbiology approach. We focus on the role of emerging technologies in the continual development of infectious disease research and highlight future possibilities in our ongoing quest to understand host-pathogen interaction.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Tissue microbiology. Schematic illustration of the development of the research areas leading to the emerging field of tissue microbiology. The base of the pyramid focuses on studies of the bacterial pathogens and cellular biology on the individual host cell types, while cellular microbiology examines the interaction between the two. Tissue microbiology joins cellular microbiology with the physiological and histological aspects. Schematic indicating the difficulty of translating cell culture studies . Experimentation includes many variables that are not included . Although essentially correct information is obtained within a given context, reductionistic models do not necessarily represent the complete picture. (Modified from reference 58 .)

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.BAI-0007-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Multiphoton imaging of bacterial infections. Uropathogenic infection in the kidney. Wild-type LT004 bacteria (green, arrow) ( = 12) can be seen colonizing the infected tubule (blue outline) within 2 h. As bacteria multiplied, shutdown of the peritubular capillaries was observed by a loss of the red plasma marker within surrounding capillaries (arrow, 6 h). At 24 h bacteria were cleared, leaving behind a scar in the tissue. The uropathogenic strain ARD41, which lacks PapG-mediated attachment, showed compromised colonization kinetics with few bacteria visible before 8 h (arrow). At 10 h, bacteria colonized the tubule lumen, and signs of vascular dysfunction appeared (arrow) ( = 12). At 24 h the bacteria were cleared, similar to the wild-type infection (panel A). Scale bars: 7 to 10 h = 30 μm, 24 h = 50 μm. (Adapted from reference 19 .) Two-photon microscopy of the epithelial layer in several adjacent villi exposed to . Some intraepithelial YFP CD103 dendritic cells were already visible at time 0, but within 30 min they were joined by several other dendritic cells that had migrated up into the epithelium (scale bar represents 50 μm). (Reprinted from reference 20 with permission from Elsevier.) Intravital multiphoton microscopy showing adhesion and extravasation of adoptively transferred neutrophils in ear dermis infected with wild-type or ΔHla . 00:00, min:s. SHG, second harmonic generation. Scale bars, 30 μm. (Adapted by permission from reference 21 . Full figure reused with permission from reference 59 .)

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.BAI-0007-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Staining of (green) biofilm extracellular matrix by luminescent conjugated oligothiophene (LCO) optotracing (red). Scale bar = 10 μm. (Adapted with permission from reference 48 .)

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.BAI-0007-2019
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error