HIGHER PERCENTAGES OF CIRCULATING MAST CELL PRECURSORS CORRELATE WITH SUSCEPTIBILITY TO REINFECTION WITH SCHISTOSOMA MANSONI

LISA M. GANLEY-LEAL Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by LISA M. GANLEY-LEAL in
Current site
Google Scholar
PubMed
Close
,
PAULINE N. M. MWINZI Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by PAULINE N. M. MWINZI in
Current site
Google Scholar
PubMed
Close
,
CATHERINE B. CETRE-SOSSAH Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by CATHERINE B. CETRE-SOSSAH in
Current site
Google Scholar
PubMed
Close
,
JULIUS ANDOVE Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by JULIUS ANDOVE in
Current site
Google Scholar
PubMed
Close
,
ALLEN W. HIGHTOWER Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by ALLEN W. HIGHTOWER in
Current site
Google Scholar
PubMed
Close
,
DIANA M. S. KARANJA Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by DIANA M. S. KARANJA in
Current site
Google Scholar
PubMed
Close
,
DANIEL G. COLLEY Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by DANIEL G. COLLEY in
Current site
Google Scholar
PubMed
Close
, and
W. EVAN SECOR Centers for Disease Control and Prevention, Division of Parasitic Diseases, Atlanta, Georgia; Kenya Medical Research Institute, Centre for Vector Biology and Control Research, Kisumu, Kenya; Center for Tropical & Emerging Global Diseases, and the Department of Microbiology, University of Georgia, Athens, GA; Division of Infectious Diseases, Boston University School of Medicine, Boston, MA

Search for other papers by W. EVAN SECOR in
Current site
Google Scholar
PubMed
Close
Restricted access

A high level of serum IgE is generally associated with human resistance to schistosomes, though the protective mechanisms of IgE remain undefined. We recently reported that whereas some individuals who are occupationally hyperexposed to Schistosoma mansoni display resistance to reinfection, others remain highly susceptible, in some cases due to HIV-1 co-infection. As IgE functions, in part, through FcεRI on mast cells, we characterized circulating CD117+ FcεRI+ mast cell precursors in this population. Surprisingly, a higher percentage of CD117+ cells correlated with a susceptible phenotype in HIV-1 seronegative participants with schistosomiasis. There was no association between percentages of peripheral CD117+ cells and susceptibility to reinfection in persons with HIV-1. Serum levels of polyclonal IgE were inversely correlated with percentages of CD117+ cells regardless of HIV-1 status. Thus, immature mast cells may affect IgE availability, or IgE may affect immature mast cells, altering the balance of host susceptibility and resistance to schistosomes.

Author Notes

  • 1

    Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA, 1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349 :243–245.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Rihet P, Demeure CE, Bourgois A, Prata A, Dessein AJ, 1991. Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur J Immunol 21 :2679–2686.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Zhang Z, Wu H, Chen S, Hu L, Xie Z, Qiu Y, Su C, Cao JP, Wu Y, Zhang S, Wu G, 1997. Association between IgE antibody against soluble egg antigen and resistance to reinfection with Schistosoma japonicum. Trans R Soc Trop Med Hyg 91 :606–608.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Demeure CE, Rihet P, Abel L, Ouattara M, Bourgois A, Dessein AJ, 1993. Resistance to Schistosoma mansoni in humans: influence of the IgE/IgG4 balance and IgG2 in immunity to reinfection after chemotherapy. J Infect Dis 168 :1000–1008.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Li Y, Sleigh AC, Ross AG, Li Y, Zhang X, Williams GM, Yu X, Tanner M, McManus DP, 2001. Human susceptibility to Schistosoma japonicum in China correlates with antibody isotypes to native antigens. Trans R Soc Trop Med Hyg 95 :441–448.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Prussin C, Metcalfe DD, 2006. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol 117 :S450–S456.

  • 7

    Mitre E, Taylor RT, Kubofcik J, Nutman TB, 2004. Parasite antigen-driven basophils are a major source of IL-4 in human filarial infections. J Immunol 172 :2439–2445.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Satti MZ, Cahen P, Skov PS, Joseph S, Jones FM, Fitzsimmons C, Hoffmann KF, Reimert C, Kariuki HC, Kazibwe F, Mwatha JK, Kimani G, Vennervald BJ, Ouma JH, Kabatereine NB, Dunne DW, 2004. Changes in IgE- and antigen-dependent histamine-release in peripheral blood of Schistosoma mansoni-infected Ugandan fishermen after treatment with praziquantel. BMC Immunol 5 :6.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Capron M, Kusnierz JP, Prin L, Spiegelberg HL, Ovlaque G, Gosset P, Tonnel AB, Capron A, 1985. Cytophilic IgE on human blood and tissue eosinophils: detection by flow microfluorometry. J Immunol 134 :3013–3018.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Ganley-Leal LM, Mwinzi PN, Cetre-Sossah CB, Andove J, High-tower AW, Karanja DM, Colley DG, Secor WE, 2006. Correlation between eosinophils and protection against reinfection with Schistosoma mansoni and the effect of human immunodeficiency virus type 1 co-infection in humans. Infect Immunol 74 :2169–2176.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Jenkins SJ, Hewitson JP, Jenkins GR, Mountford AP, 2005. Modulation of the host’s immune response by schistosome larvae. Parasite Immunol 27 :385–393.

  • 12

    Fish SC, Donaldson DD, Goldman SJ, Williams CM, Kasaian MT, 2005. IgE generation and mast cell effector function in mice deficient in IL-4 and IL-13. J Immunol 174 :7716–7724.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Bruhns P, Fremont S, Daeron M, 2005. Regulation of allergy by Fc receptors. Curr Opin Immunol 17 :662–669.

  • 14

    Gibbs BF, Wierecky J, Welker P, Henz BM, Wolff HH, Grabbe J, 2001. Human skin mast cells rapidly release preformed and newly generated TNF-alpha and IL-8 following stimulation with anti-IgE and other secretagogues. Exp Dermatol 10 :312–320.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Mitre E, Nutman TB, 2006. Basophils, basophilia and helminth infections. Chem Immunol Allergy 90 :141–156.

  • 16

    Mitre E, Nutman TB, 2003. Lack of basophilia in human parasitic infections. Am J Trop Med Hyg 69 :87–91.

  • 17

    Mitre E, Norwood S, Nutman TB, 2005. Saturation of immunoglobulin E (IgE) binding sites by polyclonal IgE does not explain the protective effect of helminth infections against atopy. Infect Immunol 73 :4106–4111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Karanja DM, Hightower AW, Colley DG, Mwinzi PN, Galil K, Andove J, Secor WE, 2002. Resistance to reinfection with Schistosoma mansoni in occupationally exposed adults and effect of HIV-1 co-infection on susceptibility to schistosomiasis: a longitudinal study. Lancet 360 :592–596.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE, 1997. Studies on schistosomiasis in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 56 :515–521.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Kirshenbaum AS, Goff JP, Semere T, Foster B, Scott LM, Metcalfe DD, 1999. Demonstration that human mast cells arise from a progenitor cell population that is CD34(+), c-kit(+), and expresses aminopeptidase N (CD13). Blood 94 :2333–2342.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Schernthaner GH, Hauswirth AW, Baghestanian M, Agis H, Ghannadan M, Worda C, Krauth MT, Printz D, Fritsch G, Sperr WR, Valent P, 2005. Detection of differentiation- and activation-linked cell surface antigens on cultured mast cell progenitors. Allergy 60 :1248–1255.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Bannert N, Farzan M, Friend DS, Ochi H, Price KS, Sodroski J, Boyce JA, 2001. Human mast cell progenitors can be infected by macrophagetropic human immunodeficiency virus type 1 and retain virus with maturation in vitro. J Virol 75 :10808–10814.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Baghestanian M, Bankl H, Sillaber C, Beil WJ, Radaszkiewicz T, Fureder W, Preiser J, Vesely M, Schernthaner G, Lechner K, Valent P, 1996. A case of malignant mastocytosis with circulating mast cell precursors: biologic and phenotypic characterization of the malignant clone. Leukemia 10 :159–166.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Li Y, Li L, Wadley R, Reddel SW, Qi JC, Archis C, Collins A, Clark E, Cooley M, Kouts S, Naif HM, Alali M, Cunningham A, Wong GW, Stevens RL, Krilis SA, 2001. Mast cells/basophils in the peripheral blood of allergic individuals who are HIV-1 susceptible due to their surface expression of CD4 and the chemokine receptors CCR3, CCR5, and CXCR4. Blood 97 :3484–3490.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Taub DD, Mikovits JA, Nilsson G, Schaffer EM, Key ML, Petrow-Sadowski C, Ruscetti FW, 2004. Alterations in mast cell function and survival following in vitro infection with human immunodeficiency viruses-1 through CXCR4. Cell Immunol 30 :65–80.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Juremalm M, Nilsson G, 2005. Chemokine receptor expression by mast cells. Chem Immunol Allergy 87 :130–144.

  • 27

    Marone G, Florio G, Petraroli A, Triggiani M, de Paulis A, 2001. Human mast cells and basophils in HIV-1 infection. Trends Immunol 22 :229–232.

  • 28

    de Paulis A, De Palma R, Di Gioia L, Carfora M, Prevete N, Tosi G, Accolla RS, Marone G, 2000. Tat protein is an HIV-1 encoded β chemokine homolog that promotes migration and up-regulations CCR3 expression on human FcεRI+ cells. J Immunol 165 :7171–7179.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Karray S, Zouali M, 1997. Identification of the B cell superantigen-binding site of HIV-1 gp120. Proc Natl Acad Sci U S A 94 :1356–1360.

  • 30

    Patella V, Florio G, Petraroli A, Marone G, 2000. HIV-1 gp120 induces IL-4 and IL-13 release from human FceRI+ cells through interaction with the VH3 region of IgE. J Immunol 164 :589–595.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Kawakami T, Kitaura J, 2005. Mast cell survival and activation by IgE in the absence of antigen: a consideration of the biologic mechanisms and relevance. J Immunol 175 :4167–4173.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Bryce PJ, Oettgen HC, 2005. Antigen-independent effects of immunoglobulin E. Curr Allergy Asthma Rep 5 :186–190.

Past two years Past Year Past 30 Days
Abstract Views 481 457 172
Full Text Views 226 4 1
PDF Downloads 39 4 1
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save