Skip to main content
SpringerLink
Log in

Th9 Cells and Parasitic Inflammation: Use of Nippostrongylus and Schistosoma Models

  • Protocol
  • First Online:
Th9 Cells

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1585))

Abstract

Th9 cells are a new subpopulation of CD4+ T helper cells, characterized by the expression of IL-9 that have been involved in type 2 immune responses, antitumor responses and autoimmune diseases. Here, we describe two different parasitic models frequently maintained in the laboratory where Th9 cells or IL-9 (the cytokine produced by Th9 cells) has been shown to play critical roles in pathogen clearance and immune response activation: the nematode Nippostrongylus brasiliensis and the trematode Schistosoma mansoni.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Lukacs NW, Strieter RM, Kunkel SL (1995) Leukocyte infiltration in allergic airway inflammation. Am J Respir Cell Mol Biol 13(1):1–6. doi:10.1165/ajrcmb.13.1.7598934

    Article  CAS  PubMed  Google Scholar 

  2. Robinson DS, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley AM, Corrigan C, Durham SR, Kay AB (1992) Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med 326(5):298–304. doi:10.1056/NEJM199201303260504

    Article  CAS  PubMed  Google Scholar 

  3. Wilhelm C, Hirota K, Stieglitz B, Van Snick J, Tolaini M, Lahl K, Sparwasser T, Helmby H, Stockinger B (2011) An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat Immunol 12(11):1071–1077. doi:10.1038/ni.2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Licona-Limon P, Henao-Mejia J, Temann AU, Gagliani N, Licona-Limon I, Ishigame H, Hao L, Herbert DR, Flavell RA (2013) Th9 Cells Drive Host Immunity against Gastrointestinal Worm Infection. Immunity 39(4):744–757. doi:10.1016/j.immuni.2013.07.020

    Article  CAS  PubMed  Google Scholar 

  5. Nicolaides NC, Holroyd KJ, Ewart SL, Eleff SM, Kiser MB, Dragwa CR, Sullivan CD, Grasso L, Zhang LY, Messler CJ, Zhou T, Kleeberger SR, Buetow KH, Levitt RC (1997) Interleukin 9: a candidate gene for asthma. Proc Natl Acad Sci U S A 94(24):13175–13180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Levitt RC, McLane MP, MacDonald D, Ferrante V, Weiss C, Zhou T, Holroyd KJ, Nicolaides NC (1999) IL-9 pathway in asthma: new therapeutic targets for allergic inflammatory disorders. J Allergy Clin Immunol 103(5 Pt 2):S485–S491

    Article  CAS  PubMed  Google Scholar 

  7. Faulkner H, Renauld JC, Van Snick J, Grencis RK (1998) Interleukin-9 enhances resistance to the intestinal nematode Trichuris muris. Infect Immun 66(8):3832–3840

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Uyttenhove C, Simpson RJ, Van Snick J (1988) Functional and structural characterization of P40, a mouse glycoprotein with T-cell growth factor activity. Proc Natl Acad Sci U S A 85(18):6934–6938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Petit-Frere C, Dugas B, Braquet P, Mencia-Huerta JM (1993) Interleukin-9 potentiates the interleukin-4-induced IgE and IgG1 release from murine B lymphocytes. Immunology 79(1):146–151

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Dugas B, Renauld JC, Pene J, Bonnefoy JY, Peti-Frere C, Braquet P, Bousquet J, Van Snick J, Mencia-Huerta JM (1993) Interleukin-9 potentiates the interleukin-4-induced immunoglobulin (IgG, IgM and IgE) production by normal human B lymphocytes. Eur J Immunol 23(7):1687–1692. doi:10.1002/eji.1830230743

    Article  CAS  PubMed  Google Scholar 

  11. Shimbara A, Christodoulopoulos P, Soussi-Gounni A, Olivenstein R, Nakamura Y, Levitt RC, Nicolaides NC, Holroyd KJ, Tsicopoulos A, Lafitte JJ, Wallaert B, Hamid QA (2000) IL-9 and its receptor in allergic and nonallergic lung disease: increased expression in asthma. J Allergy Clin Immunol 105(1 Pt 1):108–115

    Article  CAS  PubMed  Google Scholar 

  12. Schmitt E, Germann T, Goedert S, Hoehn P, Huels C, Koelsch S, Kuhn R, Muller W, Palm N, Rude E (1994) IL-9 production of naive CD4+ T cells depends on IL-2, is synergistically enhanced by a combination of TGF-beta and IL-4, and is inhibited by IFN-gamma. J Immunol 153(9):3989–3996

    CAS  PubMed  Google Scholar 

  13. Veldhoen M, Uyttenhove C, van Snick J, Helmby H, Westendorf A, Buer J, Martin B, Wilhelm C, Stockinger B (2008) Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat Immunol 9(12):1341–1346. doi:10.1038/ni.1659

    Article  CAS  PubMed  Google Scholar 

  14. Dardalhon V, Awasthi A, Kwon H, Galileos G, Gao W, Sobel RA, Mitsdoerffer M, Strom TB, Elyaman W, Ho IC, Khoury S, Oukka M, Kuchroo VK (2008) IL-4 inhibits TGF-beta-induced Foxp3+ T cells and, together with TGF-beta, generates IL-9+ IL-10+ Foxp3(−) effector T cells. Nat Immunol (12):1347–1355. doi:10.1038/ni.1677

  15. Purwar R, Schlapbach C, Xiao S, Kang HS, Elyaman W, Jiang X, Jetten AM, Khoury SJ, Fuhlbrigge RC, Kuchroo VK, Clark RA, Kupper TS (2012) Robust tumor immunity to melanoma mediated by interleukin-9-producing T cells. Nat Med 18(8):1248–1253. doi:10.1038/nm.2856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jager A, Dardalhon V, Sobel RA, Bettelli E, Kuchroo VK (2009) Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J Immunol 183(11):7169–7177. doi:10.4049/jimmunol.0901906

    Article  PubMed  PubMed Central  Google Scholar 

  17. Gerlach K, Hwang Y, Nikolaev A, Atreya R, Dornhoff H, Steiner S, Lehr HA, Wirtz S, Vieth M, Waisman A, Rosenbauer F, McKenzie AN, Weigmann B, Neurath MF (2014) TH9 cells that express the transcription factor PU.1 drive T cell-mediated colitis via IL-9 receptor signaling in intestinal epithelial cells. Nat Immunol 15(7):676–686. doi:10.1038/ni.2920

    Article  CAS  PubMed  Google Scholar 

  18. Ciccia F, Guggino G, Rizzo A, Manzo A, Vitolo B, La Manna MP, Giardina G, Sireci G, Dieli F, Montecucco CM, Alessandro R, Triolo G (2015) Potential involvement of IL-9 and Th9 cells in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 54(12):2264–2272. doi:10.1093/rheumatology/kev252

    Article  Google Scholar 

  19. Kennedy MWHW (2013) Parasitic nematodes: molecular biology, biochemistry and immunology, 2nd edn. CAB International, Wallingford

    Book  Google Scholar 

  20. Organization WH (2016) Soil transmitted helminth infections. WHO Media Center, Geneva

    Google Scholar 

  21. Urban JF Jr, Maliszewski CR, Madden KB, Katona IM, Finkelman FD (1995) IL-4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice. J Immunol 154(9):4675–4684

    CAS  PubMed  Google Scholar 

  22. Barner M, Mohrs M, Brombacher F, Kopf M (1998) Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr Biol 8(11):669–672

    Article  CAS  PubMed  Google Scholar 

  23. McKenzie GJ, Emson CL, Bell SE, Anderson S, Fallon P, Zurawski G, Murray R, Grencis R, McKenzie AN (1998) Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9(3):423–432

    Article  CAS  PubMed  Google Scholar 

  24. WHO (2016) Schistosomiasis Media center fact sheet. WHO, Geneva

    Google Scholar 

  25. Schramm G, Haas H (2010) Th2 immune response against Schistosoma mansoni infection. Microbes Infect 12(12–13):881–888. doi:10.1016/j.micinf.2010.06.001

    Article  CAS  PubMed  Google Scholar 

  26. Fallon PG, Smith P, Dunne DW (1998) Type 1 and type 2 cytokine-producing mouse CD4+ and CD8+ T cells in acute Schistosoma mansoni infection. Eur J Immunol 28(4):1408–1416

    Article  CAS  PubMed  Google Scholar 

  27. Khalil RM, Luz A, Mailhammer R, Moeller J, Mohamed AA, Omran S, Dormer P, Hultner L (1996) Schistosoma mansoni infection in mice augments the capacity for interleukin 3 (IL-3) and IL-9 production and concurrently enlarges progenitor pools for mast cells and granulocytes-macrophages. Infect Immun 64(12):4960–4966

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Fallon PG, Smith P, Richardson EJ, Jones FJ, Faulkner HC, Van Snick J, Renauld JC, Grencis RK, Dunne DW (2000) Expression of interleukin-9 leads to Th2 cytokine-dominated responses and fatal enteropathy in mice with chronic Schistosoma mansoni infections. Infect Immun 68(10):6005–6011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Townsend JM, Fallon GP, Matthews JD, Smith P, Jolin EH, McKenzie NA (2000) IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 13(4):573–583

    Article  CAS  PubMed  Google Scholar 

  30. Camberis M, Le Gros G, Urban J Jr (2003) Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus. Curr Protoc Immunol Chapter 19:Unit 19.12. doi:10.1002/0471142735.im1912s55

    PubMed  Google Scholar 

  31. Lewis FA (1998) Schistosomiasis. Current protocols in immunology. Jonh Wiley & Sons inc, New York, NY

    Google Scholar 

  32. Nawa Y, Miller HR, Hall E, Jarrett EE (1981) Adoptive transfer of total and parasite-specific IgE responses in rats infected with Nippostrongylus brasiliensis. Immunology 44(1):119–123

    CAS  PubMed  PubMed Central  Google Scholar 

  33. SM A (1997) Dialisis and concentration of protein solutions. Current protocols in immunology. Jonh Wiley & Sons inc, New York, NY

    Google Scholar 

Download references

Acknowledgment

We apologize to the researchers whose work could not be cited due to space limitations. This work was supported by the following grants from CONACYT (CB-2015-01-255287, S008-2015-2-261227) and DGAPA (IA202116-PAPIIT).

Author information

Authors and Affiliations

  1. Departamento de Biología Celular y del Desarrollo, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Ciudad Universitaria, Coyoacán, 04510, Mexico City, Mexico

    Miguel Enrique Serrano Pinto & Paula Licona-Limón

Authors
  1. Miguel Enrique Serrano Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula Licona-Limón
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paula Licona-Limón .

Editor information

Editors and Affiliations

  1. School of Bio Science, Sir JC Bose Laboratory Complex, Indian Institute of Technology, Kharagpur, West Bengal, India

    Ritobrata Goswami

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Science+Business Media LLC

About this protocol

Cite this protocol

Pinto, M.E.S., Licona-Limón, P. (2017). Th9 Cells and Parasitic Inflammation: Use of Nippostrongylus and Schistosoma Models. In: Goswami, R. (eds) Th9 Cells. Methods in Molecular Biology, vol 1585. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6877-0_18

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-6877-0_18

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-6876-3

  • Online ISBN: 978-1-4939-6877-0

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation