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Cytokine changes in colonic mucosa associated with Blastocystis spp. subtypes 1 and 3 in diarrhoea-predominant irritable bowel syndrome

  • JAVED YAKOOB (a1), ZAIGHAM ABBAS (a1), MUHAMMAD WAQAS USMAN (a1), AISHA SULTANA (a2), MUHAMMAD ISLAM (a3), SAFIA AWAN (a1), ZUBAIR AHMAD (a2), SAEED HAMID (a1) and WASIM JAFRI (a1)...
Summary

We determined cytokines (e.g. interleukin-8, 10, 12 and TNF-α) expression by peripheral blood mononuclear cells (PBMCs) and in rectal mucosa in diarrhoea-predominant irritable bowel syndrome (D-IBS) with Blastocystis spp. Eighty patients with D-IBS and Blastocystis spp. infection were classified as ‘cases’ and 80 with D-IBS without Blastocystis spp. infection were classified as ‘control’. Cases were subdivided into D-IBS and Blastocystis sp. defined type 1 (subtype-specific primer SB83) and type 3 (SB227). Stool microscopy and culture were performed. Rectal biopsies were obtained for histology and cytokines by real-time PCR for mRNA expression of cytokines. PBMCs IL-8 was similar in different groups but in type 1, IL-8mRNA was increased compared with type 3 (P = 0·001) and control (P = 0·001). In type 1, IL-10 by PBMCs had a low mean value (14·5±1·6) compared with (16·7±1·5) type 3 and (16±2·3) in controls (P<0·001 and P<0·001, respectively). In Blastocystis sp. type 1, low IL-10 was associated with lymphocyte and plasma cell infiltration (P = 0·015 and P = 0·002, respectively). In Blastocystis sp. type 1 and type 3, IL-12 was associated with goblet cell depletion 23 (85%) (P<0·001) and 8 (29%) (P = 0·037), respectively. In Blastocystis sp. type 1, low IL-10 was associated with a proinflammatory response characterized by IL-8.

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Corresponding author
* Corresponding author: Department of Medicine, Aga Khan University, PO Box 3500, Stadium Road, Karachi-74800, Pakistan. E-mail: yakoobjaved@hotmail.com
References
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Abe, N. (2004). Molecular and phylogenetic analysis of Blastocystis isolates from various hosts. Veterinary Parasitology 120, 235242.
Abe, N., Wu, Z. and Yoshikawa, H. (2003 a). Molecular characterization of Blastocystis isolates from birds by PCR with diagnostic primers and restriction fragment length polymorphism analysis of the small subunit ribosomal RNA gene. Parasitology Research 89, 393396.
Abe, N., Wu, Z. and Yoshikawa, H. (2003 b). Molecular characterization of Blastocystis isolates from primates. Veterinary Parasitology 113, 321325.
Abe, N., Wu, Z. and Yoshikawa, H. (2003 c). Zoonotic genotypes of Blastocystis hominis detected in cattle and pigs by PCR with diagnostic primers and restriction fragment length polymorphism analysis of the small subunit ribosomal RNA gene. Parasitology Research 90, 124128.
Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L. and Powrie, F. (1999). An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. Journal of Experimental Medicine 190, 9951004.
Barbara, G., De Giorgio, R., Stanghellini, V., Cremon, C. and Corinaldesi, R. (2002). A role for inflammation in irritable bowel syndrome? Gut 5, 4144.
Chadwick, V., Paulus, B., Bethwaite, P., Tie, A. and Wilson, I. (2002). Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 122, 17781783.
Chandramathi, S., Suresh, K. and Kuppusamy, U. R. (2010). Solubilized antigen of Blastocystis hominis facilitates the growth of human colorectal cancer cells, HCT116. Parasitology Research 106, 941945.
Chen, C. C., Louie, S., McCormick, B., Walker, W. A. and Shi, H. N. (2005). Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis in mice. Infection and Immunity 73, 54685481.
Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium-thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156159.
De Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G. and de Vries, J. E. (1991). Interleukin-10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. Journal of Experimental Medicine 174, 12091220.
Djuardi, Y., Sartono, E., Wibowo, H., Supali, T. and Yazdanbakhsh, M. (2010). A longitudinal study of BCG vaccination in early childhood: the development of innate and adaptive immune responses. PLoS ONE 5, e14066. doi: 10.1371/journal.pone.0014066.
Drossman, D. A. and Dumitrascu, D. L. (2006). Rome III: new standard for functional gastrointestinal disorders. Journal of Gastrointestinal and Liver Disease 15, 237242.
Drossman, D. A., Camileri, M., Mayer, E. A. and Whitehead, W. E. (2002). AGA technical review on irritable bowel syndrome. Gastroenterology 123, 21082131.
Heid, C. A., Stevens, J., Livak, K. J. and Williams, P. M. (1996). Real time quantitative PCR. Genome Research 6, 986994.
Iguchi, A., Yoshikawa, H., Yamada, M., Kimata, I. and Arizono, N. (2009). Expression of interferon gamma and proinflammatory cytokines in the cecal mucosa of rats experimentally infected with Blastocystis sp. strain RN94–9. Parasitology Research 105, 135140.
Khan, W. I., Blennerhasset, P., Ma, C., Matthaei, K. I. and Collins, S. M. (2001). Stat6 dependent goblet cell hyperplasia during intestinal nematode infection. Parasite Immunology 23, 3942.
Khan, Z. A. and Alkhalife, I. S. (2005). Prevalence of Blastocystis hominis among “healthy” food handlers in Dammam, Saudi Arabia. Journal of Egyptian Society of Parasitology 35, 395401.
Li, L. H., Zhou, X. N., Du, Z. W., Wang, X. Z., Wang, L. B., Jiang, J. Y., Yoshikawa, H., Steinmann, P., Utzinger, J., Wu, Z., Chen, J. X., Chen, S. H. and Zhang, L. (2007 a). Molecular epidemiology of human Blastocystis in a village in Yunnan province, China. Parasitology International 56, 281286.
Li, L. H., Zhang, X. P., Lv, S., Zhang, L., Yoshikawa, H., Wu, Z., Steinmann, P., Utzinger, J., Tong, X. M., Chen, S. H. and Zhou, X. N. (2007 b). Cross sectional surveys and subtype classification of human Blastocystis isolates from four epidemiological settings in China. Parasitology Research 102, 8390.
Long, H. Y., Handschack, A., König, W. and Ambrosch, A. (2001). Blastocystis hominis modulates immune responses and cytokine release in colonic epithelial cells. Parasitology Research 87, 10291030.
Mahmoud, M. S. and Saleh, W. A. (2003). Secretory and humoral antibody responses to Blastocystis hominis in symptomatic and asymptomatic human infections. Journal of the Egyptian Society of Parasitology 33, 1330.
Markell, E. K. and Udkow, M. P. (1986). Blastocystis hominis: pathogen or fellow traveller? American Journal of Tropical Medicine Hygiene 35, 10231026.
Mirza, H., Wu, Z., Kidwai, F. and Tan, K. S. (2011). A metronidazole-resistant isolate of Blastocystis spp. is susceptible to nitric oxide and downregulates intestinal epithelial inducible nitric oxide synthase by a novel parasite survival mechanism. Infection Immunity 79, 50195026.
Mirza, H., Wu, Z., Teo, J. D. and Tan, K. S. (2012). Statin pleiotropy prevents rho kinase-mediated intestinal epithelial barrier compromise induced by Blastocystis cysteine proteases. Cell Microbiology 14, 14741484.
O'Leary, C. and Quigley, E. M. (2003). Small bowel bacterial overgrowth, celiac disease and IBS: what are the associations? American Journal of Gastroenterology 98, 720722.
Olivo-Diaz, A., Romero-Valdovinos, M., Gudiño-Ramirez, A., Reyes-Gordillo, J., Jimenez-Gonzalez, D. E., Ramirez-Miranda, M. E., Martinez-Flores, W. A., Martinez-Hernandez, F., Flisser, A. and Maravilla, P. (2012). Findings related to IL-8 and IL-10 gene polymorphisms in a Mexican patient population with irritable bowel syndrome infected with Blastocystis . Parasitology Research 111, 48744891.
O'Malley, D., Dinan, T. G. and Cryan, J. F. (2010). Alterations in colonic corticotropin-releasing factor receptors in the maternally separated rat model of irritable bowel syndrome: differential effects of acute psychological and physical stressors. Peptides 3, 662670.
O'Sullivan, M., Clayton, N., Breslin, N. P., Harman, I., Bountra, C., McLaren, A. and O'Morain, C. A. (2000). Increased mast cells in the irritable bowel syndrome. Neurogastroenterology Motility 12, 449457.
Pimentel, M., Chow, E. J. and Lin, H. C. (2000). Eradication of small bowel bacterial overgrowth reduces symptoms of irritable bowel syndrome. American Journal of Gastroenterology 95, 35033506.
Ponce-Macotela, M., González-Maciel, A., Reynoso-Robles, R. and Martínez-Gordillo, M. N. (2008). Goblet cells: are they an unspecific barrier against Giardia intestinalis or a gate? Parasitology Research 102, 509513.
Powrie, F., Leach, M. W., Mauze, S., Menon, S., Caddle, L. B. and Coffman, R. L. (1994). Inhibition of Th1 responses prevents inflammatory bowel disease in SCID mice reconstituted with CD45RBhi CD4+ T cells. Immunity 1, 553562.
Puthia, M. K., Vaithilingam, A., Lu, J. and Tan, K. S. (2005). Degradation of human secretory immunoglobulin A by Blastocystis . Parasitology Research 97, 386389.
Puthia, M. K., Lu, J. and Tan, K. S. (2008). Blastocystis ratti contains cysteine proteases that mediate interleukin-8 response from human intestinal epithelial cells in an NF-kappaB-dependent manner Eukaryotic Cell 7, 435443.
Reiman, R. M., Thompson, R. W., Feng, C. G., Hari, D., Knight, R., Cheever, A. W., Rosenberg, H. F. and Wynn, T. A. (2006). Interleukin-5 (IL-5) augments the progression of liver fibrosis by regulating IL-13 activity. Infection and Immunity 74, 14711479.
Schröder, J. M., Mrowietz, U., Morita, E. and Christophers, E. (1987). Purification and partial biochemical characterization of a human monocyte-derived, neutrophil-activating peptide that lacks interleukin-1 activity. Journal of Immunology 139, 34743483.
Stensvold, R., Brillowska-Dabrowska, A., Nielsen, H. V. and Arendrup, M. C. (2006). Detection of Blastocystis hominis in unpreserved stool specimens by using polymerase chain reaction. Journal of Parasitology 92, 10811087.
Stensvold, C. R., Suresh, G. K., Tan, K. S. W., Thompson, R. C., Traub, R. J., Viscogliosi, E., Yoshikawa, H. and Clark, C. G. (2007). Terminology for Blastocystis subtypes – a consensus. Trends in Parasitology 23, 9396.
Tsukada, Y., Nakamura, T., Iimura, M., Iizuka, B. E. and Hayashi, N. (2002). Cytokine profile in colonic mucosa of ulcerative colitis correlates with disease activity and response to granulocytapheresis. American Journal of Gastroenterology 97, 28202828.
Turner, D. M., Williams, D. M., Sankaran, D., Lazarus, M., Sinnott, P. J. and Hutchinson, I. V. (1997). An investigation of polymorphism in the interleukin-10 gene promoter. European Journal of Immunogenetics 24, 18.
van der Veek, P. P., van den Berg, M., de Kroon, Y. E., Verspaget, H. W. and Masclee, A. A. (2005). Role of tumor necrosis factor-alpha and interleukin-10 gene polymorphisms in irritable bowel syndrome. American Journal of Gastroenterology 100, 25102516.
Yakoob, J., Jafri, W., Jafri, N., Khan, R., Islam, M., Beg, M. A. and Zaman, V. (2004). Irritable bowel syndrome: in search of an etiology: role of Blastocystis hominis . American Journal of Tropical Medicine Hygiene 70, 383385.
Yakoob, J., Jafri, W., Beg, M. A., Abbas, Z., Naz, S., Islam, M. and Khan, R. (2010). Irritable bowel syndrome: is it associated with genotypes of Blastocystis hominis . Parasitology Research 106, 10331038.
Yan, Y., Su, S., Ye, J., Liao, H., Ye, J., Li, X., Luo, X. and Chen, G. (2006). Genetic variability of Blastocystis hominis isolates in China. Parasitology Research 99, 597601.
Yoshikawa, H., Nagano, I., Wu, Z., Yap, E. H., Singh, M. and Takahashi, Y. (1998). Genomic polymorphism among Blastocystis hominis strains and development of subtype-specific diagnostic primers. Molecular Cellular Probes 12, 153159.
Yoshikawa, H., Abe, N., Iwasawa, M., Kitano, S., Nagano, I. and Takahashi, Y. (2000). Genomic analysis of Blastocystis hominis strains isolated from two long-term health care facilities. Journal of Clinical Microbiology 38, 13241330.
Yoshikawa, H., Abe, N. and Wu, Z. (2003). Genomic polymorphism among Blastocystis isolates and development of PCR-based identification of zoonotic isolates. Journal of Eukaryote Microbiology 50, 710717.
Yoshikawa, H., Wu, Z., Kimata, I., Iseki, M., Ali, I. K., Hossain, M. B., Zaman, V., Haque, R. and Takahashi, Y. (2004). Polymerase chain reaction based genotype classification among human Blastocystis hominis populations isolated from different countries. Parasitology Research 92, 2229.
Zaman, V. and Khan, K. (1994). A comparison of direct microscopy with culture for the diagnosis of Blastocystis hominis . Southeast Asian Journal of Tropical Medicine Hygiene Public Health 25, 792793.
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Parasitology
  • ISSN: 0031-1820
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