PI3K p110δ Is Expressed by gp38-CD31+ and gp38+CD31+ Spleen Stromal Cells and Regulates Their CCL19, CCL21, and LTβR mRNA Levels

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Zotes, Teresa M ^a   Spada, Roberto ^a   Mulens, Vladimir ^a   Pérez Yagüe, Sonia ^a   Sorzano, Carlos O ^a   Okkenhaug, Klaus ^b   Carrera, Ana C ^a   Barber, Domingo F ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; GLYCOPROTEIN; GLYCOPROTEIN GP 38; LYMPHOTOXIN BETA RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE P100DELTA; PHOSPHOTRANSFERASE; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL POPULATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLUORESCENCE ACTIVATED CELL SORTING; HEMATOPOIETIC CELL; HOMEOSTASIS; IMMUNOREGULATION; IMMUNOSTIMULATION; LYMPH NODE; LYMPHOCYTE MIGRATION; MOUSE; MUTANT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; STROMA CELL; WILD TYPE;

ANIMALS; ANTIGENS; ANTIGENS, CD31; CHEMOKINE CCL19; CHEMOKINE CCL21; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; GENE EXPRESSION REGULATION; IMMUNOPHENOTYPING; LYMPHOID TISSUE; LYMPHOTOXIN BETA RECEPTOR; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; RNA, MESSENGER; SPLEEN; STROMAL CELLS; T-LYMPHOCYTE SUBSETS; TUMOR NECROSIS FACTORS;

EID: 84883221728     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072960     Document Type: Article

References (49)

1. Mebius RE, Kraal G, (2005) Structure and function of the spleen. Nat Rev Immunol 5: 606-616.
2. Ruddle NH, Akirav EM, (2009) Secondary lymphoid organs: responding to genetic and environmental cues in ontogeny and the immune response. J Immunol 183: 2205-2212.
3. Turley SJ, Fletcher AL, Elpek KG, (2010) The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat Rev Immunol 10: 813-825.
4. Mueller SN, Germain RN, (2009) Stromal cell contributions to the homeostasis and functionality of the immune system. Nat Rev Immunol 9: 618-629.
5. Malhotra D, Fletcher AL, Turley SJ, (2013) Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity. Immunol Rev 251: 160-176.
6. Pellas TC, Weiss L, (1990) Deep splenic lymphatic vessels in the mouse: a route of splenic exit for recirculating lymphocytes. Am J Anat 187: 347-354.
7. Shimizu K, Morikawa S, Kitahara S, Ezaki T, (2009) Local lymphogenic migration pathway in normal mouse spleen. Cell Tissue Res 338: 423-32.
8. Luther SA, Tang HL, Hyman PL, Farr AG, Cyster JG, (2000) Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc Natl Acad Sci USA 97: 12694-12699.
9. Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, et al. (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8: 1255-1265.
10. Mueller SN, Ahmed R, (2008) Lymphoid stroma in the initiation and control of immune responses. Immunol Rev 224: 284-294.
11. Cyster JG, Ansel KM, Reif K, Ekland EH, Hyman PL, et al. (2000) Follicular stromal cells and lymphocyte homing to follicles. Immunol Rev 176: 181-193.
12. Katakai T, Hara T, Sugai M, Gonda H, Shimizu A, (2004) Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J Exp Med 200: 783-795.
13. den Haan JM, Mebius RE, Kraal G, (2012) Stromal cells of the mouse spleen. Front Immunol 3: 201.
14. Gunn MD, Tangemann K, Tam C, Cyster JG, Rosen SD, et al. (1998) A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc Natl Acad Sci USA 95: 258-263.
15. Gunn MD, Kyuwa S, Tam C, Kakiuchi T, Matsuzawa A, et al. (1999) Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med 189: 451-460.
16. Roozendaal R, Mempel TR, Pitcher LA, Gonzalez SF, Verschoor A, et al. (2009) Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 30: 264-276.
17. Cyster JG, (2005) Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu Rev Immunol 23: 127-159.
18. Tumanov AV, Grivennikov SI, Shakhov AN, Rybtsov SA, Koroleva EP, et al. (2003) Dissecting the role of lymphotoxin in lymphoid organs by conditional targeting. Immunol Rev 195: 106-116.
19. Randall TD, Carragher DM, Rangel-Moreno J, (2008) Development of secondary lymphoid organs. Annu Rev Immunol 26: 627-650.
20. Cyster JG, (2003) Lymphoid organ development and cell migration. Immunol Rev 195: 5-14.
21. Ngo VN, Korner H, Gunn MD, Schmidt KN, Riminton DS, et al. (1999) Lymphotoxin alpha/beta and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J Exp Med 189: 403-412.
22. Mounzer RH, Svendsen OS, Baluk P, Bergman CM, Padera TP, et al. (2010) Lymphotoxin-alpha contributes to lymphangiogenesis. Blood 116: 2173-2182.
23. So L, Fruman DA, (2012) PI3K signalling in B- and T-lymphocytes: new developments and therapeutic advances. Biochem J 442: 465-481.
24. Eickholt BJ, Ahmed AI, Davies M, Papakonstanti EA, Pearce W, et al. (2007) Control of axonal growth and regeneration of sensory neurons by the p110delta PI 3-kinase. PLoS One 2: e869.
25. Sawyer C, Sturge J, Bennett DC, O'Hare MJ, Allen WE, et al. (2003) Regulation of breast cancer cell chemotaxis by the phosphoinositide 3-kinase p110delta. Cancer Res 63: 1667-1675.
26. Geng L, Tan J, Himmelfarb E, Schueneman A, Niermann K, et al. (2004) A specific antagonist of the p110delta catalytic component of phosphatidylinositol 3′-kinase, IC486068, enhances radiation-induced tumor vascular destruction. Cancer Res 64: 4893-4899.
27. Puri KD, Doggett TA, Douangpanya J, Hou Y, Tino WT, et al. (2004) Mechanisms and implications of phosphoinositide 3-kinase delta in promoting neutrophil trafficking into inflamed tissue. Blood 103: 3448-3456.
28. Whitehead MA, Bombardieri M, Pitzalis C, Vanhaesebroeck B, (2012) Isoform-selective induction of human p110δ PI3K expression by TNFα: identification of a new and inducible PIK3CD promoter. Biochem J. 443: 857-867.
29. Puri KD, Gold MR, (2012) Selective inhibitors of phosphoinositide 3-kinase delta: modulators of B-cell function with potential for treating autoimmune inflammatory diseases and B-cell malignancies. Front Immunol 3: 256.
30. Okkenhaug K, Bilancio A, Farjot G, Priddle H, Sancho S, et al. (2002) Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 297: 1031-1034.
31. Clayton E, Bardi G, Bell SE, Chantry D, Downes CP, et al. (2002) A crucial role for the p110delta subunit of phosphatidylinositol 3-kinase in B cell development and activation. J Exp Med 196: 753-763.
32. Jou ST, Carpino N, Takahashi Y, Piekorz R, Chao JR, et al. (2002) Essential, nonredundant role for the phosphoinositide 3-kinase p110delta in signaling by the B-cell receptor complex. Mol Cell Biol 22: 8580-8591.
33. Rolf J, Bell SE, Kovesdi D, Janas ML, Soond DR, et al. (2010) Phosphoinositide 3-kinase activity in T cells regulates the magnitude of the germinal center reaction. J Immunol 185: 4042-4052.
34. Patton DT, Garden OA, Pearce WP, Clough LE, Monk CR, et al. (2006) Cutting edge: the phosphoinositide 3-kinase p110 delta is critical for the function of CD4+CD25+Foxp3+ regulatory T cells. J Immunol 177: 6598-6602.
35. Papakonstanti EA, Zwaenepoel O, Bilancio A, Burns E, Nock GE, et al. (2008) Distinct roles of class IA PI3K isoforms in primary and immortalised macrophages. J Cell Sci 121: 4124-4133.
36. Okkenhaug K, Ali K, Vanhaesebroeck B, (2007) Antigen receptor signalling: a distinctive role for the p110delta isoform of PI3K. Trends Immunol 28: 80-87.
37. Liu D, Zhang T, Marshall AJ, Okkenhaug K, Vanhaesebroeck B, et al. (2009) The p110delta isoform of phosphatidylinositol 3-kinase controls susceptibility to Leishmania major by regulating expansion and tissue homing of regulatory T cells. J Immunol 183: 1921-1933.
38. Liu D, Uzonna JE, (2010) The p110delta isoform of phosphatidylinositol 3-kinase controls the quality of secondary anti-Leishmania immunity by regulating expansion and effector function of memory T cell subsets. J Immunol 184: 3098-3105.
39. Rolf J, Bell SE, Kovesdi D, Janas ML, Soond DR, et al. (2010) Phosphoinositide 3-kinase activity in T cells regulates the magnitude of the germinal center reaction. J Immunol 185: 4042-4052.
40. Fletcher AL, Malhotra D, Acton SE, Lukacs-Kornek V, Bellemare-Pelletier A, et al. (2011) Reproducible isolation of lymph node stromal cells reveals site-dependent differences in fibroblastic reticular cells. Front Immunol 2: 35.
41. Rosati E, Scaringi L, Cornacchione P, Fettucciari K, Sabatini R, et al. (1995) Cytokine response to inactivated Candida albicans in mice. Cell Immunol 162: 256-264.
42. Scaringi L, Rosati E, Cornacchione P, Fettucciari K, Sabatini R, et al. (1995) Local and systemic immune response to inactivated Candida albicans in mice. Nat Immun 14: 234-249.
43. Aksoy E, Taboubi S, Torres D, Delbauve S, Hachani A, et al. (2012) The p110δ isoform of the kinase PI(3)K controls the subcellular compartmentalization of TLR4 signaling and protects from endotoxic shock. Nat Immunol 13: 1045-1054.
44. De Togni P, Goellner J, Ruddle NH, Streeter PR, Fick A, et al. (1994) Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264: 703-707.
45. Banks TA, Rouse BT, Kerley MK, Blair PJ, Godfrey VL, et al. (1995) Lymphotoxin-alpha-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J Immunol 155: 1685-1693.
46. Koni PA, Sacca R, Lawton P, Browning JL, Ruddle NH, et al. (1997) Distinct roles in lymphoid organogenesis for lymphotoxins alpha and beta revealed in lymphotoxin beta-deficient mice. Immunity 6: 491-500.
47. Futterer A, Mink K, Luz A, Kosco-Vilbois MH, Pfeffer K, (1998) The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 9: 59-70.
48. Ettinger R, Browning JL, Michie SA, van Ewijk W, McDevitt HO, (1996) Disrupted splenic architecture, but normal lymph node development in mice expressing a soluble lymphotoxin-beta receptor-IgG1 fusion protein. Proc Natl Acad Sci USA 93: 13102-13107.
49. Fu YX, Huang G, Matsumoto M, Molina H, Chaplin DD, (1997) Independent signals regulate development of primary and secondary follicle structure in spleen and mesenteric lymph node. Proc Natl Acad Sci USA 94: 5739-5743.