FAN (factor associated with neutral sphingomyelinase activation), a moonlighting protein in TNF-R1 signaling

Journal of Leukocyte Biology

Volumn 88, Issue 5, 2010, Pages 897-903

  Montfort, Anne ^a,b   Martin, Pascal G P ^c   Levade, Thierry ^a,b   Benoist, Hervé ^a,b,d   Ségui, Bruno ^a,b,d  

^a INSERM   (France)

^b Institut de Médecine Molé Culaire de Rangueil   (France)

^c CEMAGREF   (France)

^d UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Apoptosis; Ceramide; Immune response; Inflammation; NSMAF

Indexed keywords

ADAPTOR PROTEIN; FACTOR ASSOCIATED WITH NEUTRAL SPHINGOMYELINASE ACTIVATION; SPHINGOMYELIN PHOSPHODIESTERASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG;

APOPTOSIS; BIOLOGICAL ACTIVITY; CELL STIMULATION; CELLULAR DISTRIBUTION; CYTOTOXICITY; ENZYME ACTIVATION; IMMUNE RESPONSE; INFLAMMATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; SHORT SURVEY; SIGNAL TRANSDUCTION;

ANIMALS; AUTOIMMUNE DISEASES; ENZYME ACTIVATION; HUMANS; INFLAMMATION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR WEIGHT; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78649567621     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0410188     Document Type: Short Survey

References (67)

1. Carswell, E. A., Old, L. J., Kassel, R. L., Green, S., Fiore, N., Williamson, B. (1975) An endotoxin-induced serum factor that causes necrosis of tumors. Proc. Natl. Acad. Sci. USA 72, 3666-3670.
2. Laster, S. M., Wood, J. G., Gooding, L. R. (1988) Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J. Immunol. 141, 2629-2634.
3. Woods, K. M., Chapes, S. K. (1993) Three distinct cell phenotypes of induced-TNF cytotoxicity and their relationship to apoptosis. J. Leukoc. Biol. 53, 37-44.
4. Mannel, D. N., Echtenacher, B. (2000) TNF in the inflammatory response. Chem. Immunol. 74, 141-161.
5. Gatto, B. (2006) Biologics targeted at TNF: design, production and challenges. Reumatismo 58, 94-103.
6. Hasegawa, A., Takasaki, W., Greene, M. I., Murali, R. (2001) Modifying TNFα for therapeutic use: a perspective on the TNF receptor system. Mini Rev. Med. Chem. 1, 5-16.
7. Bradley, J. R. (2008) TNF-mediated inflammatory disease. J. Pathol. 214, 149-160.
8. Schluter, D., Kwok, L. Y., Lutjen, S., Soltek, S., Hoffmann, S., Korner, H., Deckert, M. (2003) Both lymphotoxin-α and TNF are crucial for control of Toxoplasma gondii in the central nervous system. J. Immunol. 170, 6172-6182.
9. Deckert-Schluter, M., Bluethmann, H., Rang, A., Hof, H., Schluter, D. (1998) Crucial role of TNF receptor type 1 (p55), but not of TNF receptor type 2 (p75), in murine toxoplasmosis. J. Immunol. 160, 3427-3436.
10. Rothe, J., Lesslauer, W., Lotscher, H., Lang, Y., Koebel, P., Kontgen, F., Althage, A., Zinkernagel, R., Steinmetz, M., Bluethmann, H. (1993) Mice lacking the tumor necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364, 798-802.
11. O'Brien, D. P., Briles, D. E., Szalai, A. J., Tu, A. H., Sanz, I., Nahm, M. H. (1999) Tumor necrosis factor α receptor I is important for survival from Streptococcus pneumoniae infections. Infect. Immun. 67, 595-601.
12. Le Hir, M., Bluethmann, H., Kosco-Vilbois, M. H., Muller, M., di Padova, F., Moore, M., Ryffel, B., Eugster, H. P. (1995) Tumor necrosis factor receptor- 1 signaling is required for differentiation of follicular dendritic cells, germinal center formation, and full antibody responses. J. Inflamm. 47, 76-80.
13. Le Hir, M., Bluethmann, H., Kosco-Vilbois, M. H., Muller, M., di Padova, F., Moore, M., Ryffel, B., Eugster, H. P. (1996) Differentiation of follicular dendritic cells and full antibody responses require tumor necrosis factor receptor-1 signaling. J. Exp. Med. 183, 2367-2372.
14. Pasparakis, M., Alexopoulou, L., Episkopou, V., Kollias, G. (1996) Immune and inflammatory responses in TNF α-deficient mice: a critical requirement for TNF α in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 184, 1397-1411.
15. Marino, M. W., Dunn, A., Grail, D., Inglese, M., Noguchi, Y., Richards, E., Jungbluth, A., Wada, H., Moore, M., Williamson, B., Basu, S., Old, L. J. (1997) Characterization of tumor necrosis factor-deficient mice. Proc. Natl. Acad. Sci. USA 94, 8093-8098.
16. Malagarie-Cazenave, S., Segui, B., Leveque, S., Garcia, V., Carpentier, S., Altie, M. F., Brouchet, A., Gouaze, V., Andrieu-Abadie, N., Barreira, Y., Benoist, H., Levade, T. (2004) Role of FAN in tumor necrosis factor-α and lipopolysaccharide-induced interleukin-6 secretion and lethality in D-galactosamine-sensitized mice. J. Biol. Chem. 279, 18648-18655.
17. Montfort, A., de Badts, B., Douin-Echinard, V., Martin, P. G., Iacovoni, J., Nevoit, C., Therville, N., Garcia, V., Bertrand, M. A., Bessieres, M. H., Trombe, M. C., Levade, T., Benoist, H., Segui, B. (2009) FAN stimulates TNF(α)-induced gene expression, leukocyte recruitment, and humoral response. J. Immunol. 183, 5369-5378.
18. Probert, L., Eugster, H. P., Akassoglou, K., Bauer, J., Frei, K., Lassmann, H., Fontana, A. (2000) TNFR1 signaling is critical for the development of demyelination and the limitation of T-cell responses during immune-mediated CNS disease. Brain 123, 2005-2019.
19. Hsu, H., Huang, J., Shu, H. B., Baichwal, V., Goeddel, D. V. (1996) TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity 4, 387-396.
20. Hsu, H., Shu, H. B., Pan, M. G., Goeddel, D. V. (1996) TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84, 299-308.
21. Wajant, H., Pfizenmaier, K., Scheurich, P. (2003) Tumor necrosis factor signaling. Cell Death Differ. 10, 45-65.
22. Micheau, O., Tschopp, J. (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181-190.
23. Schneider-Brachert, W., Tchikov, V., Neumeyer, J., Jakob, M., Winoto- Morbach, S., Held-Feindt, J., Heinrich, M., Merkel, O., Ehrenschwender, M., Adam, D., Mentlein, R., Kabelitz, D., Schutze, S. (2004) Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 21, 415-428.
24. Adam, D., Wiegmann, K., Adam-Klages, S., Ruff, A., Kronke, M. (1996) A novel cytoplasmic domain of the p55 tumor necrosis factor receptor initiates the neutral sphingomyelinase pathway. J. Biol. Chem. 271, 14617-14622.
25. Adam-Klages, S., Adam, D., Wiegmann, K., Struve, S., Kolanus, W., Schneider-Mergener, J., Kronke, M. (1996) FAN, a novel WD-repeat protein, couples the p55 TNF-receptor to neutral sphingomyelinase. Cell 86, 937-947.
26. Segui, B., Andrieu-Abadie, N., Adam-Klages, S., Meilhac, O., Kreder, D., Garcia, V., Bruno, A. P., Jaffrezou, J. P., Salvayre, R., Kronke, M., Levade, T. (1999) CD40 signals apoptosis through FAN-regulated activation of the sphingomyelin-ceramide pathway. J. Biol. Chem. 274, 37251-37258.
27. Kreder, D., Krut, O., Adam-Klages, S., Wiegmann, K., Scherer, G., Plitz, T., Jensen, J. M., Proksch, E., Steinmann, J., Pfeffer, K., Kronke, M. (1999) Impaired neutral sphingomyelinase activation and cutaneous barrier repair in FAN-deficient mice. EMBO J. 18, 2472-2479.
28. Zhang, Y., Kreder, D., Schwandner, R., Krut, O., Scherer, G., Adam-Klages, S., Siebert, R., Kronke, M., Schlegelberger, B. (1999) Assignment of the human FAN protein gene (NSMAF) to human chromosome region 8q12→q13 by in situ hybridization. Cytogenet. Cell Genet. 87, 115-116. (Pubitemid 30021051)
29. Semov, A., Semova, N., Lacelle, C., Marcotte, R., Petroulakis, E., Proestou, G., Wang, E. (2002) Alterations in TNF- and IL-related gene expression in space-flown WI38 human fibroblasts. FASEB J. 16, 899-901.
30. Adam-Klages, S., Schwandner, R., Adam, D., Kreder, D., Bernardo, K., Kronke, M. (1998) Distinct adapter proteins mediate acid versus neutral sphingomyelinase activation through the p55 receptor for tumor necrosis factor. J. Leukoc. Biol. 63, 678-682.
31. Tcherkasowa, A. E., Adam-Klages, S., Kruse, M. L., Wiegmann, K., Mathieu, S., Kolanus, W., Kronke, M., Adam, D. (2002) Interaction with factor associated with neutral sphingomyelinase activation, a WD motif-containing protein, identifies receptor for activated C-kinase 1 as a novel component of the signaling pathways of the p55 TNF receptor. J. Immunol. 169, 5161-5170.
32. Jogl, G., Shen, Y., Gebauer, D., Li, J., Wiegmann, K., Kashkar, H., Kronke, M., Tong, L. (2002) Crystal structure of the BEACH domain reveals an unusual fold and extensive association with a novel PH domain. EMBO J. 21, 4785-4795.
33. Haubert, D., Gharib, N., Rivero, F., Wiegmann, K., Hosel, M., Kronke, M., Kashkar, H. (2007) PtdIns(4,5)P-restricted plasma membrane localization of FAN is involved in TNF-induced actin reorganization. EMBO J. 26, 3308-3321.
34. Nagle, D. L., Karim, M. A., Woolf, E. A., Holmgren, L., Bork, P., Misumi, D. J., McGrail, S. H., Dussault Jr., B. J., Perou, C. M., Boissy, R. E., Duyk, G. M., Spritz, R. A., Moore, K. J. (1996) Identification and mutation analysis of the complete gene for Chediak-Higashi syndrome. Nat. Genet. 14, 307-311.
35. Barbosa, M. D., Nguyen, Q. A., Tchernev, V. T., Ashley, J. A., Detter, J. C., Blaydes, S. M., Brandt, S. J., Chotai, D., Hodgman, C., Solari, R. C., Lovett, M., Kingsmore, S. F. (1996) Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 382, 262-265.
36. Mohlig, H., Mathieu, S., Thon, L., Frederiksen, M. C., Ward, D. M., Kaplan, J., Schutze, S., Kabelitz, D., Adam, D. (2007) The WD repeat protein FAN regulates lysosome size independent from abnormal downregulation/membrane recruitment of protein kinase C. Exp. Cell Res. 313, 2703-2718.
37. Peppelenbosch, M., Boone, E., Jones, G. E., van Deventer, S. J., Haegeman, G., Fiers, W., Grooten, J., Ridley, A. J. (1999) Multiple signal transduction pathways regulate TNF-induced actin reorganization in macrophages: inhibition of Cdc42-mediated filopodium formation by TNF. J. Immunol. 162, 837-845.
38. Ridley, A. J. (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529.
39. Wiegmann, K., Schutze, S., Machleidt, T., Witte, D., Kronke, M. (1994) Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell 78, 1005-1015.
40. Segui, B., Andrieu-Abadie, N., Jaffrezou, J. P., Benoist, H., Levade, T. (2006) Sphingolipids as modulators of cancer cell death: potential therapeutic targets. Biochim. Biophys. Acta 1758, 2104-2120.
41. Segui, B., Cuvillier, O., Adam-Klages, S., Garcia, V., Malagarie-Cazenave, S., Leveque, S., Caspar-Bauguil, S., Coudert, J., Salvayre, R., Kronke, M., Levade, T. (2001) Involvement of FAN in TNF-induced apoptosis. J. Clin. Invest. 108, 143-151.
42. Sabourdy, F., Kedjouar, B., Sorli, S. C., Colie, S., Milhas, D., Salma, Y., Levade, T. (2008) Functions of sphingolipid metabolism in mammals - lessons from genetic defects. Biochim. Biophys. Acta 1781, 145-183.
43. Tomiuk, S., Hofmann, K., Nix, M., Zumbansen, M., Stoffel, W. (1998) Cloned mammalian neutral sphingomyelinase: functions in sphingolipid signaling? Proc. Natl. Acad. Sci. USA 95, 3638-3643.
44. Hofmann, K., Tomiuk, S., Wolff, G., Stoffel, W. (2000) Cloning and characterization of the mammalian brain-specific, Mg2+-dependent neutral sphingomyelinase. Proc. Natl. Acad. Sci. USA 97, 5895-5900.
45. Krut, O., Wiegmann, K., Kashkar, H., Yazdanpanah, B., Kronke, M. (2006) Novel tumor necrosis factor-responsive mammalian neutral sphingomyelinase-3 is a C-tail-anchored protein. J. Biol. Chem. 281, 13784-13793.
46. Wu, B. X., Rajagopalan, V., Roddy, P. L., Clarke, C. J., Hannun, Y. A. Identification and characterization of murine mitochondrial-associated neutral sphingomyelinase (ma-nsmase), the mammalian sphingomyelin phosphodiesterase 5. J. Biol. Chem., Epub ahead of print.
47. Milhas, D., Clarke, C. J., Hannun, Y. A. (2009) Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett. 584, 1887-1894.
48. Marchesini, N., Luberto, C., Hannun, Y. A. (2003) Biochemical properties of mammalian neutral sphingomyelinase 2 and its role in sphingolipid metabolism. J. Biol. Chem. 278, 13775-13783.
49. Wiegmann, K., Schwandner, R., Krut, O., Yeh, W. C., Mak, T. W., Kronke, M. (1999) Requirement of FADD for tumor necrosis factor-induced activation of acid sphingomyelinase. J. Biol. Chem. 274, 5267-5270.
50. Philipp, S., Puchert, M., Adam-Klages, S., Tchikov, V., Winoto-Morbach, S., Mathieu, S., Deerberg, A., Kolker, L., Marchesini, N., Kabelitz, D., Hannun, Y. A., Schütze, S., Adam, D. (2010) The Polycomb group protein EED couples TNF receptor 1 to neutral sphingomyelinase. Proc. Natl. Acad. Sci. USA 107, 1112-1117.
51. Tartaglia, L. A., Ayres, T. M., Wong, G. H., Goeddel, D. V. (1993) A novel domain within the 55 kd TNF receptor signals cell death. Cell 74, 845-853.
52. Neumeyer, J., Hallas, C., Merkel, O., Winoto-Morbach, S., Jakob, M., Thon, L., Adam, D., Schneider-Brachert, W., Schutze, S. (2006) TNF-receptor I defective in internalization allows for cell death through activation of neutral sphingomyelinase. Exp. Cell Res. 312, 2142-2153.
53. Werneburg, N., Guicciardi, M. E., Yin, X. M., Gores, G. J. (2004) Tumor necrosis factor-{α}-mediated lysosomal permeabilization is FAN and caspase 8/Bid-dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G436-G443.
54. O'Brien, N. W., Gellings, N. M., Guo, M., Barlow, S. B., Glembotski, C. C., Sabbadini, R. A. (2003) Factor associated with neutral sphingomyelinase activation and its role in cardiac cell death. Circ. Res. 92, 589-591. (Pubitemid 36417690)
55. Obeid, L. M., Linardic, C. M., Karolak, L. A., Hannun, Y. A. (1993) Programmed cell death induced by ceramide. Science 259, 1769-1771.
56. Granot, T., Milhas, D., Carpentier, S., Dagan, A., Segui, B., Gatt, S., Levade, T. (2006) Caspase-dependent and -independent cell death of Jurkat human leukemia cells induced by novel synthetic ceramide analogs. Leukemia 20, 392-399.
57. Schutze, S., Machleidt, T., Adam, D., Schwandner, R., Wiegmann, K., Kruse, M. L., Heinrich, M., Wickel, M., Kronke, M. (1999) Inhibition of receptor internalization by monodansylcadaverine selectively blocks p55 tumor necrosis factor receptor death domain signaling. J. Biol. Chem. 274, 10203-10212.
58. Luschen, S., Adam, D., Ussat, S., Kreder, D., Schneider-Brachert, W., Krönke, M., Adam-Klages, S. (2000) Activation of ERK1/2 and cPLA(2) by the p55 TNF receptor occurs independently of FAN. Biochem. Biophys. Res. Commun. 274, 506-512.
59. Hildt, E., Oess, S. (1999) Identification of Grb2 as a novel binding partner of tumor necrosis factor (TNF) receptor I. J. Exp. Med. 189, 1707-1714.
60. Palin, K., Bluthe, R. M., McCusker, R. H., Levade, T., Moos, F., Dantzer, R., Kelley, K. W. (2009) The type 1 TNF receptor and its associated adapter protein, FAN, are required for TNFα-induced sickness behavior. Psychopharmacology (Berl.) 201, 549-556.
61. Tian, B., Nowak, D. E., Jamaluddin, M., Wang, S., Brasier, A. R. (2005) Identification of direct genomic targets downstream of the nuclear factor-κB transcription factor mediating tumor necrosis factor signaling. J. Biol. Chem. 280, 17435-17448.
62. Larange, A., Antonios, D., Pallardy, M., Kerdine-Romer, S. (2009) TLR7 and TLR8 agonists trigger different signaling pathways for human dendritic cell maturation. J. Leukoc. Biol. 85, 673-683.
63. Ni, Z., Bremner, R. (2007) Brahma-related gene 1-dependent STAT3 recruitment at IL-6-inducible genes. J. Immunol. 178, 345-351.
64. Costa-Pereira, A. P., Tininini, S., Strobl, B., Alonzi, T., Schlaak, J. F., Is'harc, H., Gesualdo, I., Newman, S. J., Kerr, I. M., Poli, V. (2002) Mutational switch of an IL-6 response to an interferon-γ-like response. Proc. Natl. Acad. Sci. USA 99, 8043-8047.
65. Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Bluethmann, H., Kohler, G. (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368, 339-342. (Pubitemid 24104268)
66. Tan, N. S., Michalik, L., Noy, N., Yasmin, R., Pacot, C., Heim, M., Fluhmann, B., Desvergne, B., Wahli, W. (2001) Critical roles of PPAR β/δ in keratinocyte response to inflammation. Genes Dev. 15, 3263-3277.
67. Sanchez, C., Rueda, D., Segui, B., Galve-Roperh, I., Levade, T., Guzman, M. (2001) The CB(1) cannabinoid receptor of astrocytes is coupled to sphingomyelin hydrolysis through the adaptor protein fan. Mol. Pharmacol. 59, 955-959.