Leptin receptor mutation results in defective neutrophil recruitment to the colon during Entamoeba histolytica infection

mBio

Volumn 5, Issue 6, 2014, Pages

  Naylor, Caitlin ^a   Burgess, Stacey ^a   Madan, Rajat ^b   Buonomo, Erica ^a   Razzaq, Khadija ^a   Ralston, Katherine ^c   Petri, William A ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; GRANULOCYTE COLONY STIMULATING FACTOR; LEPTIN RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; LEPTIN RECEPTOR, HUMAN; LEPTIN RECEPTOR, MOUSE;

AMEBIASIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CECUM; CELL DEATH; CELL FUNCTION; CELL INFILTRATION; CELL SELECTION; CELL TRANSPORT; CONTROLLED STUDY; INFECTION SENSITIVITY; INNATE IMMUNITY; MALE; MOUSE; MUTATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PARASITE CLEARANCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CHEMOTAXIS; COLON; DISEASE MODEL; DISEASE PREDISPOSITION; ENTAMOEBA HISTOLYTICA; GENETICS; HUMAN; IMMUNOLOGY; MISSENSE MUTATION; NEUTROPHIL; PHYSIOLOGY;

ENTAMOEBA HISTOLYTICA; MUS;

ANIMALS; CHEMOTAXIS; COLON; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; ENTAMOEBA HISTOLYTICA; ENTAMOEBIASIS; HUMANS; MICE; MUTATION, MISSENSE; NEUTROPHIL INFILTRATION; NEUTROPHILS; RECEPTORS, LEPTIN;

EID: 84920969940     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02046-14     Document Type: Article

References (35)

1. Haque R, Huston CD, Hughes M, Houpt E, Petri WA. 2003. Amebiasis. N. Engl. J. Med. 348:1565-1573. http://dx.doi.org/10.1056/NEJMra022710.
2. Taniuchi M, Sobuz SU, Begum S, Platts-Mills JA, Liu J, Yang Z, Wang XQ, Petri WA, Haque R, Houpt ER. 2013. Etiology of diarrhea in Bangladeshi infants in the first year of life analyzed using molecular methods. J. Infect. Dis. 208:1794-1802. http://dx.doi.org/10.1093/infdis/jit507.
3. Mortimer L, Chadee K. 2010. The immunopathogenesis of Entamoeba histolytica. Exp. Parasitol. 126:366-380. http://dx.doi.org/10.1016/j.exppara.2010.03.005.
4. Duggal P, Guo X, Haque R, Peterson KM, Ricklefs S, Mondal D, Alam F, Noor Z, Verkerke HP, Marie C, Leduc CA, Chua SC, Myers MG, Leibel RL, Houpt E, Gilchrist CA, Sher A, Porcella SF, Petri WA. 2011. A mutation in the leptin receptor is associated with Entamoeba histolytica infection in children. J. Clin. Invest. 121:1191-1198. http://dx.doi.org/10.1172/JCI45294.of.
5. Verkerke H, Naylor C, Zabeau L, Tavernier J, Petri Wa, Marie C. 2014. Kinetics of leptin binding to the Q223R leptin receptor. PLoS One 9:e94843. http://dx.doi.org/10.1371/journal.pone.0094843.
6. Marie CS, Verkerke HP, Paul SN, Mackey AJ, Petri WA. 2012. Leptin protects host cells from Entamoeba histolytica cytotoxicity by a STAT3- dependent mechanism. Infect. Immun. 80:1934-1943. http://dx.doi.org/10.1128/IAI.06140-11.
7. Margetic S, Gazzola C, Pegg GG, Hill RA. 2002. Leptin: a review of its peripheral actions and interactions. Int. J. Obes. Relat. Metab. Disord. 26:1407-1433. http://dx.doi.org/10.1038/sj.ijo.0802142.
8. Faggioni R, Feingold KR, Grunfeld C. 2001. Leptin regulation of the immune response and the immunodeficiency of malnutrition. FASEB J. 15:2565-2571. http://dx.doi.org/10.1096/fj.01-0431rev.
9. Petri WA, Mondal D, Peterson KM, Duggal P, Haque R. 2009. Association of malnutrition with amebiasis. Nutr. Rev. 67(Suppl 2):S207-S215. http://dx.doi.org/10.1111/j.1753-4887.2009.00242.x.
10. Fernández-Riejos P, Najib S, Santos-Alvarez J, Martín-Romero C, Pérez-Pérez A, González-Yanes C, Sánchez-Margalet V. 2010, 2010. Role of leptin in the activation of immune cells. Mediators Inflamm. 2010: 568343. http://dx.doi.org/10.1155/2010/568343.
11. Mackey-Lawrence NM, Guo X, Sturdevant DE, Virtaneva K, Hernandez MM, Houpt E, Sher A, Porcella SF, Petri WA. 2013. Effect of the leptin receptor Q223R polymorphism on the host transcriptome following infection with Entamoeba histolytica. Infect. Immun. 81:1460-1470. http://dx.doi.org/10.1128/IAI.01383-12.
12. Houpt ER, Glembocki DJ, Obrig TG, Moskaluk CA, Lockhart LA, Wright RL, Seaner RM, Keepers TR, Wilkins TD, Petri WA. 2002. The mouse model of amebic colitis reveals mouse strain susceptibility to infection and exacerbation of disease by CD4+ T cells. J. Immunol. 169: 4496-4503. http://dx.doi.org/10.4049/jimmunol.169.8.4496.
13. Ralston KS, Solga MD, Mackey-lawrence NM, Somlata A, Bhattacharya A, Petri WA. 2014. Trogocytosis by Entamoeba histolytica contributes to cell killing and tissue invasion. Nature 508:526-530. http://dx.doi.org/10.1038/nature13242.
14. Bracho-Riquelme RL, Loera-Castañeda V, Torres-Valenzuela A, Loera- Castañeda GA, Sánchez-Ramírez JP. 2011. Leptin and leptin receptor polymorphisms are associated with poor outcome (death) in patients with non-appendicular secondary peritonitis. Crit. Care 15:R227. http://dx.doi.org/10.1186/cc10467.
15. Wang B, Fu E, Cao Y, Zhong Y, Fu G, Tian X, Li S. 2013. Effect of leptin receptor mutation on the development of chronic bronchitis. Asia Pac. J. Public Health 25(4 Suppl):80S-87S. http://dx.doi.org/10.1177/1010539513497218.
16. Asgharpour A, Gilchrist C, Baba D, Hamano S, Houpt E. 2005. Resistance to intestinal Entamoeba histolytica infection is conferred by innate immunity and Gr-1+ cells. Infect. Immun. 73:4522-4529. http://dx.doi.org/10.1128/IAI.73.8.4522.
17. Chadee K. 1989. Human neutrophils activated by interferon-y and tumour necrosis factor-+ kill Entamoeba histolytica trophozoites. In Vitro 274:270-274.
18. Guo X, Roberts MR, Becker SM, Podd B, Zhang Y, Chua SC, Myers MG, Duggal P, Houpt ER, Petri WA. 2011. Leptin signaling in intestinal epithelium mediates resistance to enteric infection by Entamoeba histolytica. Mucosal Immunol. 4:294-303. http://dx.doi.org/10.1038/mi.2010.76.
19. Yang SK, Eckmann L, Panja A, Kagnoff MF. 1997. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113:1214-1223. doi:10.1053/gast.1997.v 13.pm9322516. PubMed.
20. Sitaraman S, Liu X, Charrier L, Gu LH, Ziegler TR, Gewirtz A, Merlin D. 2004. Colonic leptin: source of a novel pro-inflammatory cytokine involved in inflammatory bowel disease. FASEB J. 18:696-698. http://dx.doi.org/10.1096/fj.03-0422fje.
21. Song F, Ito K, Denning TL, Kuninger D, Papaconstantinou J, Gourley W, Klimpel G, Balish E, Hokanson J, Ernst PB. 1999. Expression of the neutrophil chemokine KC in the colon of mice with enterocolitis and by intestinal epithelial cell lines: effects of flora and proinflammatory cytokines. J. Immunol. 162:2275-2280.
22. Ohtsuka Y, Lee J, Stamm DS, Sanderson IR. 2001. MIP-2 secreted by epithelial cells increases neutrophil and lymphocyte recruitment in the mouse intestine. Gut 49:526-533. http://dx.doi.org/10.1136/gut.49.4.526.
23. Ogunwobi OO, Beales IL. 2007. The anti-apoptotic and growth stimulatory actions of leptin in human colon cancer cells involves activation of JNK mitogen activated protein kinase, JAK2 and PI3 kinase/Akt. Int. J. Colorectal Dis. 22:401-409. http://dx.doi.org/10.1007/s00384-006-0181-y.
24. Bruno A, Conus S, Schmid I, Simon HU. 2005. Apoptotic pathways are inhibited by leptin receptor activation in neutrophils. J. Immunol. 174: 8090-8096. http://dx.doi.org/10.4049/jimmunol.174.12.8090.
25. Papathanassoglou E, El-haschimi K, Li XC, Matarese G, Strom T, Mantzoros C. 2006. Leptin receptor expression and signaling in lymphocytes: kinetics during lymphocyte activation, role in lymphocyte survival, and response to high fat diet in mice. J. Immunol. 176: 7745-7752. http://dx.doi.org/10.4049/jimmunol.176.12.7745.
26. Azuma T, Suto H, Ito Y, Ohtani M, Dojo M, Kuriyama M, Kato T. 2001. Gastric leptin and Helicobacter pylori infection. Gut 49:324-329. http://dx.doi.org/10.1136/gut.49.3.324.
27. Ubags ND, Vernooy JH, Burg E, Hayes C, Bement J, Dilli E, Zabeau L, Abraham E, Poch KR, Nick JA, Dienz O, Zuñiga J, Wargo MJ, Mizgerd JP, Tavernier J, Rincón M, Poynter ME, Wouters EF, Suratt BT. 2014. The role of leptin in the development of pulmonary neutrophilia in infection and acute lung injury. Crit. Care Med. 42:e143-e151. http://dx.doi.org/10.1097/CCM.0000000000000048.
28. Moshyedi AK, Josephs MD, Abdalla EK, Mackay SL, Edwards CK, Copeland EM, Moldawer LL. 1998. Increased leptin expression in mice with bacterial peritonitis is partially regulated by tumor necrosis factor alpha. Infect. Immun. 66:1800-1802.
29. Siegl D, Annecke T, Johnson BL, Schlag C, Martignoni A, Huber N, Conzen P, Caldwell CC, Tschöp J. 2014. Obesity-induced hyperleptinemia improves survival and immune response in a murine model of sepsis. Anesthesiology 121:98-114. http://dx.doi.org/10.1097/ALN.0000000000000192.
30. Zarkesh-Esfahani H, Pockley AG, Wu Z, Hellewell PG, Weetman AP, Ross RJ. 2004. Leptin indirectly activates human neutrophils via induction of TNF-alpha. J. Immunol. 172:1809-1814. http://dx.doi.org/10.4049/jimmunol.172.3.1809.
31. Montecucco F, Bianchi G, Gnerre P, Bertolotto M, Dallegri F, Ottonello L. 2006. Induction of neutrophil chemotaxis by leptin: crucial role for p38 and Src kinases. Ann. N. Y. Acad. Sci. 1069:463-471. http://dx.doi.org/10.1196/annals.1351.045.
32. Caldefie-Chezet F, Poulin A, Vasson MP. 2003. Leptin regulates functional capacities of polymorphonuclear neutrophils. Free Radic. Res. 37: 809-814. http://dx.doi.org/10.1080/1071576031000097526.
33. Summers C, Rankin SM, Condliffe AM, Singh N, Peters AM, Chilvers ER. 2010. Neutrophil kinetics in health and disease. Trends Immunol. 31:318-324. http://dx.doi.org/10.1016/j.it.2010.05.006.
34. Caldefie-Chezet F, Poulin A, Tridon A, Sion B, Vasson MP. 2001. Leptin: a potential regulator of polymorphonuclear neutrophil bactericidal action? J. Leukoc. Biol. 69:414-418.
35. Rodríguez L, Graniel J, Ortiz R. 2007. Effect of leptin on activation and cytokine synthesis in peripheral blood lymphocytes of malnourished infected children. Clin. Exp. Immunol. 148:478-485. http://dx.doi.org/10.1111/j.1365-2249.2007.03361.x.