Effect of the leptin receptor Q223R polymorphism on the host transcriptome following infection with Entamoeba histolytica

Infection and Immunity

Volumn 81, Issue 5, 2013, Pages 1460-1470

  Mackey Lawrence, Nicole M ^a   Guo, Xiaoti ^a,b   Sturdevant, Daniel E ^c   Virtaneva, Kimmo ^c   Hernandez, Matthew M ^c   Houpt, Eric ^a   Sher, Alan ^d   Porcella, Stephen F ^c   Petri, William A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b North Shore Long Island Health System ^*  (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN RECEPTOR; Q223R PROTEIN; STAT3 PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ALLELE; AMEBIASIS; ANIMAL EXPERIMENT; ARTICLE; BACTERIUM CULTURE; CELL PROLIFERATION; CODON; GENE EXPRESSION; GENOTYPE; INFECTION SENSITIVITY; INTESTINE INFECTION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN POLYMORPHISM;

EID: 84877835708     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01383-12     Document Type: Article

References (73)

1. Ozata M, Ozdemir IC, Licinio J. 1999. Human leptin deficiency caused by a missense mutation: multiple endocrine defects, decreased sympathetic tone, and immune system dysfunction indicate new targets for leptin action, greater central than peripheral resistance to the effects of leptin, and spontaneous correction of leptin-mediated defects. J. Clin. Endocrinol. Metab. 84:3686 -3695.
2. Farooqi IS, Wangensteen T, Collins S, Kimber W, Matarese G, Keogh JM, Lank E, Bottomley B, Lopez-Fernandez J, Ferraz-Amaro I, Dattani MT, Ercan O, Myhre AG, Retterstol L, Stanhope R, Edge JA, McKenzie S, Lessan N, Ghodsi M, De Rosa V, Perna F, Fontana S, Barroso I, Undlien DE, O'Rahilly S. 2007. Clinical and molecular genetic spectrum of congenital deficiency of the leptin receptor. N. Engl. J. Med. 356:237- 247.
3. Mackey-Lawrence NM, Petri WA, Jr. 2012. Leptin and mucosal immunity. Mucosal Immunol. 5:472- 479.
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, Jr, Myers MG, Jr, Leibel RL, Houpt E, Gilchrist CA, Sher A, Porcella SF, Petri WA, Jr. 2011. A mutation in the leptin receptor is associated with Entamoeba histolytica infection in children. J. Clin. Invest. 121:1191-1198.
5. Guo X, Roberts MR, Becker SM, Podd B, Zhang Y, Chua SC, Jr, Myers MG, Jr, Duggal P, Houpt ER, Petri WA, Jr. 2011. Leptin signaling in intestinal epithelium mediates resistance to enteric infection by Entamoeba histolytica. Mucosal Immunol. 4:294 -303.
6. Fruhbeck G. 2006. Intracellular signalling pathways activated by leptin. Biochem. J. 393:7-20.
7. Leinninger GM, Myers MG, Jr. 2008. LRb signals act within a distributed network of leptin-responsive neurones to mediate leptin action. Acta Physiol. 192:49 -59.
8. Myers MG, Jr. 2004. Leptin receptor signaling and the regulation of mammalian physiology. Recent Prog. Horm. Res. 59:287-304.
9. Marie CS, Verkerke HP, Paul SN, Mackey AJ, Petri WA, Jr. 2012. Leptin protects host cells from Entamoeba histolytica cytotoxicity by a STAT3- dependent mechanism. Infect. Immun. 80:1934 -1943.
10. Gove ME, Pini M, Fayad R, Cabay RJ, Fantuzzi G. 2009. Adiponectin deficiency modulates adhesion molecules expression and cytokine production but does not affect disease severity in the transfer model of colitis. Cytokine 47:119 -125.
11. Hruz P, Dann SM, Eckmann L. 2010. STAT3 and its activators in intestinal defense and mucosal homeostasis. Curr. Opin. Gastroenterol. 26: 109-115.
12. Li Y, de Haar C, Chen M, Deuring J, Gerrits MM, Smits R, Xia B, Kuipers EJ, van der Woude CJ. 2010. Disease-related expression of the IL6/STAT3/SOCS3 signalling pathway in ulcerative colitis and ulcerative colitis-related carcinogenesis. Gut 59:227-235.
13. Pickert G, Neufert C, Leppkes M, Zheng Y, Wittkopf N, Warntjen M, Lehr HA, Hirth S, Weigmann B, Wirtz S, Ouyang W, Neurath MF, Becker C. 2009. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206:1465-1472.
14. Agrawal S, Gollapudi S, Su H, Gupta S. 2011. Leptin activates human B cells to secrete TNF-alpha, IL-6, and IL-10 via JAK2/STAT3 and p38MAPK/ERK1/2 signaling pathway. J. Clin. Immunol. 31:472- 478.
15. Stratigopoulos G, LeDuc CA, Matsuoka N, Gutman R, Rausch R, Robertson SA, Myers MG, Jr, Chung WK, Chua SC, Jr, Leibel RL. 2009. Functional consequences of the human leptin receptor (LEPR) Q223R transversion. Obesity (Silver Spring) 17:126 -135.
16. Houpt ER, Glembocki DJ, Obrig TG, Moskaluk CA, Lockhart LA, Wright RL, Seaner RM, Keepers TR, Wilkins TD, Petri WA, Jr. 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.
17. Graham MR, Virtaneva K, Porcella SF, Barry WT, Gowen BB, Johnson CR, Wright FA, Musser JM. 2005. Group A Streptococcus transcriptome dynamics during growth in human blood reveals bacterial adaptive and survival strategies. Am. J. Pathol. 166:455- 465.
18. Klipper-Aurbach Y, Wasserman M, Braunspiegel-Weintrob N, Borstein D, Peleg S, Assa S, Karp M, Benjamini Y, Hochberg Y, Laron Z. 1995. Mathematical formulae for the prediction of the residual beta cell function during the first two years of disease in children and adolescents with insulin- dependent diabetes mellitus. Med. Hypotheses 45:486-490.
19. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207-210.
20. Val S, Belade E, George I, Boczkowski J, Baeza-Squiban A. 2012. Fine PM induce airway MUC5AC expression through the autocrine effect of amphiregulin. Arch. Toxicol. 86:1851-1859.
21. Wilson KJ, Mill C, Lambert S, Buchman J, Wilson TR, Hernandez- Gordillo V, Gallo RM, Ades LM, Settleman J, Riese DJ, II. 2012. EGFR ligands exhibit functional differences in models of paracrine and autocrine signaling. Growth Factors 30:107-116.
22. Scheller J, Chalaris A, Garbers C, Rose-John S. 2011. ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 32:380 -387.
23. Westlund J, Livingston M, Fahlen-Yrlid L, Oldenborg PA, Yrlid U. 2012. CD47-deficient mice have decreased production of intestinal IgA following oral immunization but a maintained capacity to induce oral tolerance. Immunology 135:236 -244.
24. Grahnert A, Grahnert A, Klein C, Schilling E, Wehrhahn J, Hauschildt S. 2011. NAD: a modulator of immune functions. Innate Immun. 17: 212-233.
25. Slomiany BL, Slomiany A. 2009. Leptin-induced cytosolic phospholipase A2 activation in gastric mucosal protection against ethanol cytotoxicity involves epidermal growth factor receptor transactivation. Inflammopharmacology 17:6 -14.
26. Shang K, Bai YP, Wang C, Wang Z, Gu HY, Du X, Zhou XY, Zheng CL, Chi YY, Mukaida N, Li YY. 2012. Crucial involvement of tumorassociated neutrophils in the regulation of chronic colitis-associated carcinogenesis in mice. PLoS One 7:e51848. doi:10.1371/journal.pone .0051848.
27. Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J. 2009. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J. Leukoc. Biol. 86:557-566.
28. Foell D, Wittkowski H, Ren Z, Turton J, Pang G, Daebritz J, Ehrchen J, Heidemann J, Borody T, Roth J, Clancy R. 2008. Phagocyte-specific S100 proteins are released from affected mucosa and promote immune responses during inflammatory bowel disease. J. Pathol. 216:183-192.
29. Foell D, Wittkowski H, Vogl T, Roth J. 2007. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J. Leukoc. Biol. 81:28 -37.
30. Tew DG, Southan C, Rice SQ, Lawrence MP, Li H, Boyd HF, Moores K, Gloger IS, Macphee CH. 1996. Purification, properties, sequencing, and cloning of a lipoprotein-associated, serine-dependent phospholipase involved in the oxidative modification of low-density lipoproteins. Arterioscler. Thromb. Vasc. Biol. 16:591-599.
31. Tjoelker LW, Eberhardt C, Unger J, Trong HL, Zimmerman GA, McIntyre TM, Stafforini DM, Prescott SM, Gray PW. 1995. Plasma platelet-activating factor acetylhydrolase is a secreted phospholipase A2 with a catalytic triad. J. Biol. Chem. 270:25481-25487.
32. Merched A, Tollefson K, Chan L. 2010. Beta2 integrins modulate the initiation and progression of atherosclerosis in low-density lipoprotein receptor knockout mice. Cardiovasc. Res. 85:853- 863.
33. Simon AJ, Lev A, Wolach B, Gavrieli R, Amariglio N, Rosenthal E, Gazit E, Eyal E, Rechavi G, Somech R. 2010. The effect of gentamicininduced readthrough on a novel premature termination codon of CD18 leukocyte adhesion deficiency patients. PLoS One 5:e13659. doi:10.1371 /journal.pone.0013659.
34. Gordon S, Hamann J, Lin HH, Stacey M. 2011. F4/80 and the related adhesion-GPCRs. Eur. J. Immunol. 41:2472-2476.
35. Van Lint P, Libert C. 2007. Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J. Leukoc. Biol. 82:1375-1381.
36. Price NM, Gilman RH, Uddin J, Recavarren S, Friedland JS. 2003. Unopposed matrix metalloproteinase-9 expression in human tuberculous granuloma and the role of TNF-alpha-dependent monocyte networks. J. Immunol. 171:5579 -5586.
37. Wang M, Qin X, Mudgett JS, Ferguson TA, Senior RM, Welgus HG. 1999. Matrix metalloproteinase deficiencies affect contact hypersensitivity: stromelysin-1 deficiency prevents the response and gelatinase B deficiency prolongs the response. Proc. Natl. Acad. Sci. U. S. A. 96:6885- 6889.
38. Hirschey MD, Shimazu T, Jing E, Grueter CA, Collins AM, Aouizerat B, Stancakova A, Goetzman E, Lam MM, Schwer B, Stevens RD, Muehlbauer MJ, Kakar S, Bass NM, Kuusisto J, Laakso M, Alt FW, Newgard CB, Farese RV, Jr, Kahn CR, Verdin E. 2011. SIRT3 deficiencyand mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol. Cell 44:177-190.
39. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG. 2011. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 29:71-109.
40. Roelle S, Grosse R, Aigner A, Krell HW, Czubayko F, Gudermann T. 2003. Matrix metalloproteinases 2 and 9 mediate epidermal growth factor receptor transactivation by gonadotropin-releasing hormone. J. Biol. Chem. 278:47307- 47318.
41. Lee CG, Da Silva CA, Dela Cruz CS, Ahangari F, Ma B, Kang MJ, He CH, Takyar S, Elias JA. 2011. Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu. Rev. Physiol. 73:479 -501.
42. Chen CC, Pekow J, Llado V, Kanneganti M, Lau CW, Mizoguchi A, Mino-Kenudson M, Bissonnette M, Mizoguchi E. 2011. Chitinase 3-like-1 expression in colonic epithelial cells as a potentially novel marker for colitis-associated neoplasia. Am. J. Pathol. 179:1494 -1503.
43. Dela Cruz CS, Liu W, He CH, Jacoby A, Gornitzky A, Ma B, Flavell R, Lee CG, Elias JA. 2012. Chitinase 3-like-1 promotes Streptococcus pneumoniae killing and augments host tolerance to lung antibacterial responses. Cell Host Microbe 12:34-46.
44. Janssens S, Tschopp J. 2006. Signals from within: the DNA-damageinduced NF-kappaB response. Cell Death Differ. 13:773-784. 45. Campbell KJ, Perkins ND. 2004. Reprogramming RelA. Cell Cycle 3:869-872.
45. Campbell KJ, Perkins ND. 2004. Reprogramming RelA. Cell Cycle 3:869-872.
46. Shao Y, Aplin AE. 2010. Akt3-mediated resistance to apoptosis in B-RAFtargeted melanoma cells. Cancer Res. 70:6670-6681.
47. Yang ZZ, Tschopp O, Di-Poi N, Bruder E, Baudry A, Dummler B, Wahli W, Hemmings BA. 2005. Dosage-dependent effects of Akt1/ protein kinase Balpha (PKBalpha) and Akt3/PKBgamma on thymus, skin, and cardiovascular and nervous system development in mice. Mol. Cell. Biol. 25:10407-10418.
48. Ding L, Biswas S, Morton RE, Smith JD, Hay N, Byzova TV, Febbraio M, Podrez EA. 2012. Akt3 deficiency in macrophages promotes foam cell formation and atherosclerosis in mice. Cell Metab. 15:861- 872.
49. Wang Y, Rao VK, Kok WK, Roy DN, Sethi S, Ling BM, Lee MB, Taneja R. 2012. SUMO modification of Stra13 is required for repression of cyclin D1 expression and cellular growth arrest. PLoS One 7:e43137. doi:10.1371 /journal.pone.0043137.
50. Yun Z, Maecker HL, Johnson RS, Giaccia AJ. 2002. Inhibition of PPAR gamma 2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev. Cell 2:331- 341.
51. Shen M, Yoshida E, Yan W, Kawamoto T, Suardita K, Koyano Y, Fujimoto K, Noshiro M, Kato Y. 2002. Basic helix-loop-helix protein DEC1 promotes chondrocyte differentiation at the early and terminal stages. J. Biol. Chem. 277:50112-50120.
52. Nousbeck J, Sarig O, Avidan N, Indelman M, Bergman R, Ramon M, Enk CD, Sprecher E. 2010. Insulin-like growth factor-binding protein 7 regulates keratinocyte proliferation, differentiation and apoptosis. J. Investig. Dermatol. 130:378 -387.
53. Kolattukudy PE, Niu J. 2012. Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/CCR2 pathway. Circ.Res. 110:174 -189.
54. Menezes-Souza D, Guerra-Sa R, Carneiro CM, Vitoriano-Souza J, Giunchetti RC, Teixeira-Carvalho A, Silveira-Lemos D, Oliveira GC, Correa-Oliveira R, Reis AB. 2012. Higher expression of CCL2, CCL4, CCL5, CCL21, and CXCL8 chemokines in the skin associated with parasite density in canine visceral leishmaniasis. PLoS Negl. Trop. Dis. 6:e1566. doi:10.1371/journal.pntd.0001566.
55. Satelli A, Li S. 2011. Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell. Mol. Life Sci. 68:3033-3046.
56. Nobuhisa I, Kato R, Inoue H, Takizawa M, Okita K, Yoshimura A, Taga T. 2004. Spred-2 suppresses aorta-gonad-mesonephros hematopoiesis by inhibiting MAP kinase activation. J. Exp. Med. 199:737-742.
57. Taniguchi K, Kohno R, Ayada T, Kato R, Ichiyama K, Morisada T, Oike Y, Yonemitsu Y, Maehara Y, Yoshimura A. 2007. Spreds are essential for embryonic lymphangiogenesis by regulating vascular endothelial growth factor receptor 3 signaling. Mol. Cell. Biol. 27:4541- 4550.
58. Rojas-Lopez AE, Soldevila G, Meza-Perez S, Dupont G, Ostoa-Saloma P, Wurbel MA, Ventura-Juarez J, Flores-Romo L, Garcia-Zepeda EA. 2012. CCR9 T cells contribute to the resolution of the inflammatory response in a mouse model of intestinal amoebiasis. Immunobiology 217: 795-807.
59. Guo X, Barroso L, Lyerly DM, Petri WA, Jr, Houpt ER. 2011. CD4 and CD8T cell- and IL-17-mediated protection against Entamoeba histolytica induced by a recombinant vaccine. Vaccine 29:772-777.
60. Guo X, Stroup SE, Houpt ER. 2008. Persistence of Entamoeba histolytica infection in CBA mice owes to intestinal IL-4 production and inhibition of protective IFN-gamma. Mucosal Immunol. 1:139 -146.
61. Mortimer L, Chadee K. 2010. The immunopathogenesis of Entamoeba histolytica. Exp. Parasitol. 126:366 -380.
62. Peterson KM, Shu J, Duggal P, Haque R, Mondal D, Petri WA, Jr. 2010. Association between TNF-alpha and Entamoeba histolytica diarrhea. Am. J. Trop. Med. Hyg. 82:620-625.
63. Ralston KS, Petri WA. 2011. The ways of a killer: how does Entamoeba histolytica elicit host cell death? Essays Biochem. 51:193-210.
64. Ralston KS, Petri WA, Jr. 2011. Tissue destruction and invasion by Entamoeba histolytica. Trends Parasitol. 27:254 -263.
65. Boettner DR, Petri WA. 2005. Entamoeba histolytica activates host cell caspases during contact-dependent cell killing. Curr. Top. Microbiol. Immunol. 289:175-184.
66. Becker SM, Cho KN, Guo X, Fendig K, Oosman MN, Whitehead R, Cohn SM, Houpt ER. 2010. Epithelial cell apoptosis facilitates Entamoeba histolytica infection in the gut. Am. J. Pathol. 176:1316 -1322.
67. Lourenssen S, Houpt ER, Chadee K, Blennerhassett MG. 2010. Entamoeba histolytica infection and secreted proteins proteolytically damage enteric neurons. Infect. Immun. 78:5332-5340.
68. Guo X, Houpt E, Petri WA, Jr. 2007. Crosstalk at the initial encounter: interplay between host defense and ameba survival strategies. Curr. Opin. Immunol. 19:376 -384.
69. Bansal D, Ave P, Kerneis S, Frileux P, Boche O, Baglin AC, Dubost G, Leguern AS, Prevost MC, Bracha R, Mirelman D, Guillen N, Labruyere E. 2009. An ex-vivo human intestinal model to study Entamoeba histolytica pathogenesis. PLoS Negl. Trop. Dis. 3:e551. doi:10.1371/journal .pntd.0000551.
70. Baxt LA, Singh U. 2008. New insights into Entamoeba histolytica pathogenesis. Curr. Opin. Infect. Dis. 21:489-494.
71. Chan JL, Bluher S, Yiannakouris N, Suchard MA, Kratzsch J, Mantzoros CS. 2002. Regulation of circulating soluble leptin receptor levels by gender, adiposity, sex steroids, and leptin: observational and interventional studies in humans. Diabetes 51:2105-2112.
72. Smith JT, Waddell BJ. 2003. Developmental changes in plasma leptin and hypothalamic leptin receptor expression in the rat: peripubertal changes and the emergence of sex differences. J. Endocrinol. 176:313-319.
73. Hickey MS, Israel RG, Gardiner SN, Considine RV, McCammon MR, Tyndall GL, Houmard JA, Marks RH, Caro JF. 1996. Gender differences in serum leptin levels in humans. Biochem. Mol. Med. 59:1- 6.