Adaptive Immunity Alters Distinct Host Feeding Pathways during Nematode Induced Inflammation, a Novel Mechanism in Parasite Expulsion

PLoS Pathogens

Volumn 9, Issue 1, 2013, Pages

  Worthington, John J ^a   Samuelson, Linda C ^b   Grencis, Richard K ^a   McLaughlin, John T ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ; CYTOKINE; LEPTIN; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CD4+ T LYMPHOCYTE; CELL HYPERPLASIA; CONTROLLED STUDY; ENTERITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FOOD INTAKE; HISTOLOGY; HYPOPHAGIA; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MOUSE; MYOSITIS; NONHUMAN; TRICHINELLA SPIRALIS; TRICHINOSIS;

ADAPTIVE IMMUNITY; ANIMALS; EATING DISORDERS; ENTERITIS; FEEDING BEHAVIOR; HOST SPECIFICITY; HOST-PARASITE INTERACTIONS; INTESTINAL DISEASES, PARASITIC; MICE; MICE, KNOCKOUT; TRICHINELLA SPIRALIS; TRICHINELLOSIS; WEIGHT LOSS;

EID: 84875083047     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003122     Document Type: Article

References (41)

1. Hartman C, Eliakim R, Shamir R, (2009) Nutritional status and nutritional therapy in inflammatory bowel diseases. World Journal of Gastroenterology 15: 2570-2578.
2. Faro CJ, Reidelberger RD, Palmer JM, (2000) Suppression of food intake is linked to enteric inflammation in nematode-infected rats. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 278: R118-R124.
3. Yang S, Gaafar SM, Bottoms GD, (1990) Effects of Multiple Dose Infections with Ascaris-Suum on Blood Gastrointestinal Hormone Levels in Pigs. Veterinary Parasitology 37: 31-44.
4. Dynes RA, Poppi DP, Barrell GK, Sykes AR, (1998) Elevation of feed intake in parasite-infected lambs by central administration of a cholecystokinin receptor antagonist. British Journal of Nutrition 79: 47-54.
5. Best L, McLaughlin J, (2005) Nutrients as regulators of endocrine and neuroendocrine secretion. Topical Current Genetics 7: 79-111.
6. McDermott JR, Bartram RE, Knight PA, Miller HRP, Garrod DR, et al. (2003) Mast cells disrupt epithelial barrier function during enteric nematode infection. Proceedings of the National Academy of Sciences of the United States of America 100: 7761-7766.
7. McDermott JR, Leslie FC, D'Amato M, Thompson DG, Grencis RK, et al. (2006) Immune control of food intake: enteroendocrine cells are regulated by CD4(+) T lymphocytes during small intestinal inflammation. Gut 55: 492-497.
8. Lay JM, Gillespie PJ, Samuelson LC, (1999) Murine prenatal expression of cholecystokinin in neural crest, enteric neurons, and enteroendocrine cells. Developmental Dynamics 216: 190-200.
9. Khan WI, Ghia JE, (2010) Gut hormones: emerging role in immune activation and inflammation. Clinical and Experimental Immunology 161: 19-27.
10. McDermott JR, Humphreys NE, Forman SP, Donaldson DD, Grencis RK, (2005) Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. Journal of Immunology 175: 3207-3213.
11. Garside P, Grencis RK, Mowat AM, (1992) Lymphocyte-T Dependent Enteropathy in Murine Trichinella- Spiralis Infection. Parasite Immunology 14: 217-225.
12. Fabre MV, Beiting DP, Bliss SK, Appleton JA, (2009) Immunity to Trichinella spiralis muscle infection. Vet Parasitol 159: 245-248.
13. Wu Z, Nagano I, Boonmars T, Takahashi A, (2005) Tumor necrosis factor receptor-mediated apoptosis in Trichinella spiralis-infected muscle cells. Parasitology 131: 373-381.
14. Truyens C, Torrico F, Lucas R, De Baetselier P, Buurman WA, et al. (1999) The endogenous balance of soluble tumor necrosis factor receptors and tumor necrosis factor modulates cachexia and mortality in mice acutely infected with Trypanosoma cruzi. Infection and Immunity 67: 5579-5586.
15. Brunet LR, Finkelman FD, Cheever AW, Kopf MA, Pearce EJ, (1997) IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. Journal of Immunology 159: 777-785.
16. De SK, Devadas K, Notkins AL, (2002) Elevated levels of tumor necrosis factor alpha (TNF-alpha) in human immunodeficiency virus type 1-transgenic mice: Prevention of death by antibody to TNF-alpha. Journal of Virology 76: 11710-11714.
17. El-Shewy KA, Eid RA, (2005) In vivo killing of Giardia trophozoites harbouring bacterial endosymbionts by intestinal Paneth cells: an ultrastructural study. Parasitology 130: 269-274.
18. Hasnain SZ, Evans CE, Roy M, Gallagher AL, Kindrachuk KN, et al. (2011) Muc5ac: a critical component mediating the rejection of enteric nematodes. Journal of Experimental Medicine 208: 893-900.
19. Fernandez-Riejos P, Najib S, Santos-Alvarez J, Martin-Romero C, Perez-Perez A, et al. (2010) Role of Leptin in the Activation of Immune Cells. Mediators of Inflammation 8: 568343.
20. Barker IK, (1975) Intestinal pathology associated with Trichostrongylus colubriformis infection in sheep: histology. Parasitology 70: 165-171.
21. Lo CM, Samuelson LC, Chambers JB, King A, Heiman J, et al. (2008) Characterization of mice lacking the gene for cholecystokinin. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 294: R803-R810.
22. Lacourse KA, Swanberg LJ, Gillespie PJ, Rehfeld JF, Saunders TL, et al. (1999) Pancreatic function in CCK-deficient mice: adaptation to dietary protein does not require CCK. American Journal of Physiology-Gastrointestinal and Liver Physiology 276: G1302-G1309.
23. Wang HQ, Steeds J, Motomura Y, Deng YK, Verma-Gandhu M, et al. (2007) CD4(+) T cell-mediated immunological control of enterochromaffin cell hyperplasia and 5-hydroxytryptamine production in enteric infection. Gut 56: 949-957.
24. Bogunovic M, Dave SH, Tilstra JS, Chang DTW, Harpaz N, et al. (2007) Enteroendocrine cells express functional Toll-like receptors. American Journal of Physiology-Gastrointestinal and Liver Physiology 292: G1770-G1783.
25. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, et al. (2005) Notch signals control the fate of immature progenitor cells in the intestine. Nature 435: 964-968.
26. O'Hara JR, Sharkey KA, (2007) Proliferative capacity of enterochromaffin cells in guinea-pigs with experimental ileitis. Cell and Tissue Research 329: 433-441.
27. Langhans W, Hrupka B, (1999) Interleukins and tumor necrosis factor as inhibitors of food intake. Neuropeptides 33: 415-424.
28. PlataSalaman CR, Sonti G, Borkoski JP, Wilson CD, French Mullen JMH, (1996) Anorexia induced by chronic central administration of cytokines at estimated pathophysiological concentrations. Physiology & Behavior 60: 867-875.
29. Miller AJ, Hopkins SJ, Luheshi GN, (1997) Sites of action of IL-1 in the development of fever and cytokine responses to tissue inflammation in the rat. British Journal of Pharmacology 120: 1274-1279.
30. Karmańska K, Houszka M, Widyma A, Stefaniak E, (1997) Macrophages during infection with Trichinella spiralis in mice. Wiad Parazytol 43: 245-249.
31. Luyer MD, Greve JWM, Hadfoune M, Jacobs JA, Dejong CH, et al. (2005) Nutritional stimulation of cholecystokinin receptors inhibits inflammation via the vagus nerve. Journal of Experimental Medicine 202: 1023-1029.
32. Batra A, Okur B, Glauben R, Erben U, Ihbe J, et al. (2009) Leptin: A Critical Regulator of CD4(+) T-cell Polarization in Vitro and in Vivo. Endocrinology 151: 56-62.
33. Lo C-M, King A, Samuelson LC, Kindel TL, Rider T, et al. (2010) Cholecystokinin Knockout Mice Are Resistant to High-Fat Diet-Induced Obesity. Gastroenterology 138: 1997-2005.
34. Guo X, Roberts MR, Becker SM, Podd B, Zhang Y, et al. (2011) Leptin signaling in intestinal epithelium mediates resistance to enteric infection by Entamoeba histolytica. Mucosal Immunology 4: 294-303.
35. Mancuso P, Gottschalk A, Phare SM, Peters-Golden M, Lukacs NW, et al. (2002) Leptin-deficient mice exhibit impaired host defense in gram-negative pneumonia. Journal of Immunology 168: 4018-4024.
36. Ikejima S, Sasaki S, Sashinami H, Mori F, Ogawa Y, et al. (2005) Impairment of host resistance to Listeria monocytogenes infection in liver of db/db and ob/ob mice. Diabetes 54: 182-189.
37. Pennock JL, Grencis RK, (2006) The mast cell and gut nematodes: damage and defence. Chem Immunol Allergy 90: 128-140.
38. Taildeman J, Perez-Novo CA, Rottiers I, Ferdinande L, Waeytens A, et al. (2009) Human mast cells express leptin and leptin receptors. Histochem Cell Biol 131: 703-711.
39. Peschon JJ, Torrance DS, Stocking KL, Glaccum MB, Otten C, et al. (1998) TNF receptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation. Journal of Immunology 160: 943-952.
40. Wakelin D, Lloyd M, (1976) Accelerated expulsion of adult Trichinella spiralis in mice given lymphoid cells and serum from infected donors. Parasitology 72: 307-315.
41. Lord GM, Matarese G, Howard LK, Baker RJ, Bloom SR, et al. (1998) Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394: 897-901.