Three-dimensional tissue assemblies

Novel models for the study of Salmonella enterica serovar typhimurium pathogenesis

Cheryl Nickerson, T. J. Goodwin, J. Terlonge, C. M. Ott, K. L. Buchanan, W. C. Uicker, K. Emami, C. L. LeBlanc, R. Ramamurthy, M. S. Clarke, C. R. Vanderburg, T. Hammond, D. L. Pierson

Research output: Contribution to journalArticle

88 Citations (Scopus)

Abstract

The lack of readily available experimental systems has limited knowledge pertaining to the development of Salmonella-induced gastroenteritis and diarrheal disease in humans. We used a novel low-shear stress cell culture system developed at the National Aeronautics and Space Administration in conjunction with cultivation of three-dimensional (3-D) aggregates of human intestinal tissue to study the infectivity of Salmonella enterica serovar Typhimurium for human intestinal epithelium. Immunohistochemical characterization and microscopic analysis of 3-D aggregates of the human intestinal epithelial cell line Int-407 revealed that the 3-D cells more accurately modeled human in vivo differentiated tissues than did conventional monolayer cultures of the same cells. Results from infectivity studies showed that Salmonella established infection of the 3-D cells in a much different manner than that observed for monolayers. Following the same time course of infection with Salmonella, 3-D Int-407 cells displayed minimal loss of structural integrity compared to that of Int-407 monolayers. Furthermore, Salmonella exhibited significantly lower abilities to adhere to, invade, and induce apoptosis of 3-D Int-407 cells than it did for infected Int-407 monolayers. Analysis of cytokine expression profiles of 3-D Int-407 cells and monolayers following infection with Salmonella revealed significant differences in expression of interleukin 1α (IL-1α), IL-1β, IL-6, IL-1Ra, and tumor necrosis factor alpha mRNAs between the two cultures. In addition, uninfected 3-D Int-407 cells constitutively expressed higher levels of transforming growth factor β1 mRNA and prostaglandin E2 than did uninfected Int-407 monolayers. By more accurately modeling many aspects of human in vivo tissues, the 3-D intestinal cell model generated in this study offers a novel approach for studying microbial infectivity from the perspective of the host-pathogen interaction.

Original languageEnglish (US)
Pages (from-to)7106-7120
Number of pages15
JournalInfection and Immunity
Volume69
Issue number11
DOIs
StatePublished - 2001
Externally publishedYes

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Salmonella enterica
Salmonella Infections
Somatostatin-Secreting Cells
Interleukin-1
Salmonella
Cell Culture Techniques
United States National Aeronautics and Space Administration
Interleukin 1 Receptor Antagonist Protein
Host-Pathogen Interactions
Messenger RNA
Gastroenteritis
Transforming Growth Factors
Intestinal Mucosa
Dinoprostone
Serogroup
Interleukin-6
Tumor Necrosis Factor-alpha
Epithelial Cells
Apoptosis
Cytokines

ASJC Scopus subject areas

  • Immunology

Cite this

Three-dimensional tissue assemblies : Novel models for the study of Salmonella enterica serovar typhimurium pathogenesis. / Nickerson, Cheryl; Goodwin, T. J.; Terlonge, J.; Ott, C. M.; Buchanan, K. L.; Uicker, W. C.; Emami, K.; LeBlanc, C. L.; Ramamurthy, R.; Clarke, M. S.; Vanderburg, C. R.; Hammond, T.; Pierson, D. L.

In: Infection and Immunity, Vol. 69, No. 11, 2001, p. 7106-7120.

Research output: Contribution to journalArticle

Nickerson, C, Goodwin, TJ, Terlonge, J, Ott, CM, Buchanan, KL, Uicker, WC, Emami, K, LeBlanc, CL, Ramamurthy, R, Clarke, MS, Vanderburg, CR, Hammond, T & Pierson, DL 2001, 'Three-dimensional tissue assemblies: Novel models for the study of Salmonella enterica serovar typhimurium pathogenesis', Infection and Immunity, vol. 69, no. 11, pp. 7106-7120. https://doi.org/10.1128/IAI.69.11.7106-7120.2001
Nickerson, Cheryl ; Goodwin, T. J. ; Terlonge, J. ; Ott, C. M. ; Buchanan, K. L. ; Uicker, W. C. ; Emami, K. ; LeBlanc, C. L. ; Ramamurthy, R. ; Clarke, M. S. ; Vanderburg, C. R. ; Hammond, T. ; Pierson, D. L. / Three-dimensional tissue assemblies : Novel models for the study of Salmonella enterica serovar typhimurium pathogenesis. In: Infection and Immunity. 2001 ; Vol. 69, No. 11. pp. 7106-7120.
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