Calpain A modulates Toll responses by limited Cactus/IκB proteolysis

Molecular Biology of the Cell

Volumn 24, Issue 18, 2013, Pages 2966-2980

  Fontenele, Marcio ^a   Lim, Bomyi ^b   Oliveira, Danielle ^c   Buffolo, Márcio ^a   Perlman, David H ^c   Schupbach, Trudi ^c,d   Araujo, Helena ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular INCT EM CNPq   (Brazil)

^c PRINCETON UNIVERSITY   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CACTUS PROTEIN; CALPAIN; CALPAIN A; COPPER SULFATE; CYSTEINE PROTEINASE; DIPTERICIN; DROSOMYCIN; EGTAZIC ACID; GREEN FLUORESCENT PROTEIN; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IONOMYCIN; RNA; TOLL LIKE RECEPTOR; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM BINDING; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; ESCHERICHIA COLI; IMMUNE SYSTEM; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SURVIVAL; TRANSGENE; VERTEBRATE; WESTERN BLOTTING;

ANIMALS; BODY PATTERNING; CALPAIN; CELL LINE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FAT BODY; I-KAPPA B PROTEINS; IMMUNE SYSTEM; LARVA; MODELS, BIOLOGICAL; MUTATION; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEOLYSIS; TOLL-LIKE RECEPTORS;

EID: 84884484385     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-02-0113     Document Type: Article

References (90)

1. Anderson KV, Jurgens G, Nusslein-Volhard C (1985). Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42, 779-789. (Pubitemid 16083719)
2. Araujo H, Negreiros E, Bier E (2003). Integrins modulate Sog activity in the Drosophila wing. Development 130, 3851-3864.
3. Asha H, Nagy I, Kovacs G, Stetson D, Ando I, Dearolf CR (2003). Analysis of Ras-induced overproliferation in Drosophila hemocytes. Genetics 163, 203-215. (Pubitemid 36222665)
4. Baghdiguian S et al. (1999). Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IkappaB alpha/NF-kappaB pathway in limb-girdle muscular dystrophy type 2A. Nat Med 5, 503-511. (Pubitemid 29220208)
5. Baud V, Derudder E (2011). Control of NF-kappaB activity by proteolysis. Curr Top Microbiol Immunol 349, 97-114.
6. Belvin MP, Anderson KV (1996). A conserved signaling pathway: the Drosophila Toll-dorsal pathway. Annu Rev Cell Dev Biol 12, 393-416. (Pubitemid 26422719)
7. Belvin MP, Jin Y, Anderson KV (1995). Cactus protein degradation mediates Drosophila dorsal-ventral signaling. Genes Dev 9, 783-793.
8. Bergmann A, Stein D, Geisler R, Hagenmaier S, Schmid B, Fernandez N, Schnell B, Nusslein-Volhard C (1996). A gradient of cytoplasmic Cactus degradation establishes the nuclear localization gradient of the dorsal morphogen in Drosophila. Mech Dev 60, 109-123. (Pubitemid 27008253)
9. Bertipaglia I, Carafoli E (2007). Calpains and human disease. Subcell Biochem 45, 29-53.
10. Calle Y, Carragher NO, Thrasher AJ, Jones GE (2006). Inhibition of calpain stabilises podosomes and impairs dendritic cell motility. J Cell Sci 119, 2375-2385. (Pubitemid 43960326)
11. Chan KT, Bennin DA, Huttenlocher A (2010). Regulation of adhesion dynamics by calpain-mediated proteolysis of focal adhesion kinase (FAK). J Biol Chem 285, 11418-11426.
12. Charatsi I, Luschnig S, Bartoszewski S, Nusslein-Volhard C, Moussian B (2003). Krapfen/dMyd88 is required for the establishment of dorsoventral pattern in the Drosophila embryo. Mech Dev 120, 219-226. (Pubitemid 36143739)
13. Chen F et al. (2007). Rapsyn interaction with calpain stabilizes AChR clusters at the neuromuscular junction. Neuron 55, 247-260. (Pubitemid 47048911)
14. Choe KM, Werner T, Stoven S, Hultmark D, Anderson KV (2002). Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296, 359-362. (Pubitemid 34303693)
15. Chung K, Kim Y, Kanodia JS, Gong E, Shvartsman SY, Lu H (2011). A microfluidic array for large-scale ordering and orientation of embryos. Nat Methods 8, 171-176.
16. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B (2002). The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J 21, 2568-2579. (Pubitemid 34619373)
17. de Thonel A, Ferraris SE, Pallari HM, Imanishi SY, Kochin V, Hosokawa T, Hisanaga S, Sahlgren C, Eriksson JE (2010). Protein kinase Czeta regulates Cdk5/p25 signaling during myogenesis. Mol Biol Cell 21, 1423-1434.
18. DeLotto R, DeLotto Y, Steward R, Lippincott-Schwartz J (2007). Nucleocytoplasmic shuttling mediates the dynamic maintenance of nuclear Dorsal levels during Drosophila embryogenesis. Development 134, 4233-4241.
19. Drier EA, Huang LH, Steward R (1999). Nuclear import of the Drosophila Rel protein Dorsal is regulated by phosphorylation. Genes Dev 13, 556-568. (Pubitemid 29131880)
20. duVerle D, Takigawa I, Ono Y, Sorimachi H, Mamitsuka H (2010). CaMPDB: a resource for calpain and modulatory proteolysis. Genome Inform 22, 202-213.
21. Emori Y, Saigo K (1994). Calpain localization changes in coordination with actin-related cytoskeletal changes during early embryonic development of Drosophila. J Biol Chem 269, 25137-25142. (Pubitemid 24311785)
22. Ferguson SB, Blundon MA, Klovstad MS, Schupbach T (2012). Modulation of gurken translation by insulin and TOR signaling in Drosophila. J Cell Sci 125, 1407-1419.
23. Fernandez NQ, Grosshans J, Goltz JS, Stein D (2001). Separable and redundant regulatory determinants in Cactus mediate its dorsal group dependent degradation. Development 128, 2963-2974. (Pubitemid 32771628)
24. Foe VE, Alberts BM (1983). Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61, 31-70. (Pubitemid 13064305)
25. Fontenele M, Carneiro K, Agrellos R, Oliveira D, Oliveira-Silva A, Vieira V, Negreiros E, Machado E, Araujo H (2009). The Ca2+-dependent protease Calpain A regulates Cactus/I kappaB levels during Drosophila development in response to maternal Dpp signals. Mech Dev 126, 737-751.
26. Friedrich P, Bozoky Z (2005). Digestive versus regulatory proteases: on calpain action in vivo. Biol Chem 386, 609-612. (Pubitemid 41448163)
27. Friedrich P, Tompa P, Farkas A (2004). The calpain-system of Drosophila melanogaster: coming of age. Bioessays 26, 1088-1096. (Pubitemid 39424812)
28. Geisler R, Bergmann A, Hiromi Y, Nusslein-Volhard C (1992). cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the I kappa B gene family of vertebrates. Cell 71, 613-621.
29. Georgel P, Naitza S, Kappler C, Ferrandon D, Zachary D, Swimmer C, Kopczynski C, Duyk G, Reichhart JM, Hoffmann JA (2001). Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev Cell 1, 503-514. (Pubitemid 33586102)
30. Gillespie SK, Wasserman SA (1994). Dorsal, a Drosophila Rel-like protein, is phosphorylated upon activation of the transmembrane protein Toll. Mol Cell Biol 14, 3559-3568.
31. Govind S, Brennan L, Steward R (1993). Homeostatic balance between dorsal and cactus proteins in the Drosophila embryo. Development 117, 135-148. (Pubitemid 23094163)
32. Han Y, Weinman S, Boldogh I, Walker RK, Brasier AR (1999). Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation. J Biol Chem 274, 787-794.
33. Hecht PM, Anderson KV (1993). Genetic characterization of tube and pelle, genes required for signaling between Toll and dorsal in the specification of the dorsal-ventral pattern of the Drosophila embryo. Genetics 135, 405-417. (Pubitemid 23307596)
34. Hoffmann JA (2003). The immune response of Drosophila. Nature 426, 33-38. (Pubitemid 37432534)
35. Horng T, Medzhitov R (2001). Drosophila MyD88 is an adapter in the Toll signaling pathway. Proc Natl Acad Sci USA 98, 12654-12658. (Pubitemid 33020001)
36. Huang HR, Chen ZJ, Kunes S, Chang GD, Maniatis T (2010). Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc Natl Acad Sci USA 107, 8322-8327.
37. Ip YT, Reach M, Engstrom Y, Kadalayil L, Cai H, Gonzalez-Crespo S, Tatei K, Levine M (1993). Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell 75, 753-763. (Pubitemid 23346373)
38. Isoda K, Nusslein-Volhard C (1994). Disulfide cross-linking in crude embryonic lysates reveals three complexes of the Drosophila morphogen dorsal and its inhibitor cactus. Proc Natl Acad Sci USA 91, 5350-5354. (Pubitemid 24174324)
39. Jekely G, Friedrich P (1999). The evolution of the calpain family as reflected in paralogous chromosome regions. J Mol Evol 49, 272-281. (Pubitemid 29357869)
40. Kaczmarek JS, Riccio A, Clapham DE (2012). Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proc Natl Acad Sci USA 109, 7888-7892.
41. Kanodia JS, Rikhy R, Kim Y, Lund VK, DeLotto R, Lippincott-Schwartz J, Shvartsman SY (2009). Dynamics of the Dorsal morphogen gradient. Proc Natl Acad Sci USA 106, 21707-21712.
42. Kidd S (1992). Characterization of the Drosophila cactus locus and analysis of interactions between cactus and dorsal proteins. Cell 71, 623-635.
43. Kim Y, Andreu MJ, Lim B, Chung K, Terayama M, Jimenez G, Berg CA, Lu H, Shvartsman SY (2011). Gene regulation by MAPK substrate competition. Dev Cell 20, 880-887.
44. Kokai E, Paldy FS, Somogyi K, Chougule A, Pal M, Kerekes E, Deak P, Friedrich P, Dombradi V, Adam G (2012). CalpB modulates border cell migration in Drosophila egg chambers. BMC Dev Biol 12, 20.
45. Lade A, Ranganathan S, Luo J, Monga SP (2012). Calpain induces N-terminal truncation of beta-catenin in normal murine liver development: diagnostic implications in hepatoblastomas. J Biol Chem 287, 22789-22798.
46. Lemaitre B, Kromer-Metzger E, Michaut L, Nicolas E, Meister M, Georgel P, Reichhart JM, Hoffmann JA (1995). A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci USA 92, 9465-9469.
47. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996). The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983. (Pubitemid 26336801)
48. Lemaitre B, Reichhart JM, Hoffmann JA (1997). Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 94, 14614-14619. (Pubitemid 28041422)
49. Liberman LM, Reeves GT, Stathopoulos A (2009). Quantitative imaging of the Dorsal nuclear gradient reveals limitations to threshold-dependent patterning in Drosophila. Proc Natl Acad Sci USA 106, 22317-22322.
50. Li C, Chen S, Yue P, Deng X, Lonial S, Khuri FR, Sun SY (2010). Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IkappaB(alpha) degradation. J Biol Chem 285, 16096-16104.
51. Li G, Iyengar R (2002). Calpain as an effector of the Gq signaling pathway for inhibition of Wnt/beta -catenin-regulated cell proliferation. Proc Natl Acad Sci USA 99, 13254-13259.
52. Ligoxygakis P, Pelte N, Hoffmann JA, Reichhart JM (2002). Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 297, 114-116. (Pubitemid 34743106)
53. Liu ZP, Galindo RL, Wasserman SA (1997). A role for CKII phosphorylation of the cactus PEST domain in dorsoventral patterning of the Drosophila embryo. Genes Dev 11, 3413-3422. (Pubitemid 28023963)
54. Lu Y, Wu LP, Anderson KV (2001). The antibacterial arm of the Drosophila innate immune response requires an IkappaB kinase. Genes Dev 15, 104-110. (Pubitemid 32060686)
55. Lund VK, DeLotto Y, DeLotto R (2010). Endocytosis is required for Toll signaling and shaping of the Dorsal/NF-kappaB morphogen gradient during Drosophila embryogenesis. Proc Natl Acad Sci USA 107, 18028-18033.
56. Manfruelli P, Reichhart JM, Steward R, Hoffmann JA, Lemaitre B (1999). A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. EMBO J 18, 3380-3391. (Pubitemid 29276584)
57. Marek LR, Kagan JC (2012). Phosphoinositide binding by the Toll adaptor dMyD88 controls antibacterial responses in Drosophila. Immunity 36, 612-622.
58. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N (2008). Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 40, 476-483. (Pubitemid 351450875)
59. Meng X, Khanuja BS, Ip YT (1999). Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev 13, 792-797. (Pubitemid 29169838)
60. Michel T, Reichhart JM, Hoffmann JA, Royet J (2001). Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414, 756-759. (Pubitemid 34000773)
61. Moncrieffe MC, Grossmann JG, Gay NJ (2008). Assembly of oligomeric death domain complexes during Toll receptor signaling. J Biol Chem 283, 33447-33454.
62. Moussian B, Roth S (2005). Dorsoventral axis formation in the Drosophila embryo-shaping and transducing a morphogen gradient. Curr Biol 15, R887-R899. (Pubitemid 41566134)
63. Nicolas E, Reichhart JM, Hoffmann JA, Lemaitre B (1998). In vivo regulation of the IkappaB homologue cactus during the immune response of Drosophila. J Biol Chem 273, 10463-10469. (Pubitemid 28227656)
64. O'Dea EL, Barken D, Peralta RQ, Tran KT, Werner SL, Kearns JD, Levchenko A, Hoffmann A (2007). A homeostatic model of IkappaB metabolism to control constitutive NF-kappaB activity. Mol Syst Biol 3, 111.
65. Osman D, Gobert V, Ponthan F, Heidenreich O, Haenlin M, Waltzer L (2009). A Drosophila model identifies calpains as modulators of the human leukemogenic fusion protein AML1-ETO. Proc Natl Acad Sci USA 106, 12043-12048.
66. Packman LC, Kubota K, Parker J, Gay NJ (1997). Casein kinase II phosphorylates Ser468 in the PEST domain of the Drosophila IkappaB homologue cactus. FEBS Lett 400, 45-50. (Pubitemid 27046819)
67. Pando MP, Verma IM (2000). Signal-dependent and -independent degradation of free and NF-kappa B-bound IkappaBalpha. J Biol Chem 275, 21278-21286. (Pubitemid 30481825)
68. Park MW, Emori Y (2008). Drosophila Calpain B is monomeric and autolyzes intramolecularly. J Biochem 143, 217-228. (Pubitemid 351238163)
69. Pianetti S, Arsura M, Romieu-Mourez R, Coffey RJ, Sonenshein GE (2001). Her-2/neu overexpression induces NF-kappaB via a PI3-kinase/Akt pathway involving calpain-mediated degradation of IkappaB-alpha that can be inhibited by the tumor suppressor PTEN. Oncogene 20, 1287-1299. (Pubitemid 32269934)
70. Reach M, Galindo RL, Towb P, Allen JL, Karin M, Wasserman SA (1996). A gradient of cactus protein degradation establishes dorsoventral polarity in the Drosophila embryo. Dev Biol 180, 353-364. (Pubitemid 26426182)
71. Reeves GT, Trisnadi N, Truong TV, Nahmad M, Katz S, Stathopoulos A (2012). Dorsal-ventral gene expression in the Drosophila embryo reflects the dynamics and precision of the dorsal nuclear gradient. Dev Cell 22, 544-557.
72. Roth S (2001). Drosophila oogenesis: coordinating germ line and soma. Curr Biol 11, R779-R781. (Pubitemid 32931003)
73. Roth S, Hiromi Y, Godt D, Nusslein-Volhard C (1991). cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. Development 112, 371-388.
74. Rutschmann S, Kilinc A, Ferrandon D (2002). Cutting edge: the toll pathway is required for resistance to gram-positive bacterial infections in Drosophila. J Immunol 168, 1542-1546. (Pubitemid 34135746)
75. Schaecher K, Goust JM, Banik NL (2004). The effects of calpain inhibition on IkB alpha degradation after activation of PBMCs: identification of the calpain cleavage sites. Neurochem Res 29, 1443-1451. (Pubitemid 39011333)
76. Schiffmann DA, White JH, Cooper A, Nutley MA, Harding SE, Jumel K, Solari R, Ray KP, Gay NJ (1999). Formation and biochemical characterization of tube/pelle death domain complexes: critical regulators of postreceptor signaling by the Drosophila toll receptor. Biochemistry 38, 11722-11733.
77. Schupbach T, Wieschaus E (1989). Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics 121, 101-117.
78. Shelton CA, Wasserman SA (1993). pelle encodes a protein kinase required to establish dorsoventral polarity in the Drosophila embryo. Cell 72, 515-525. (Pubitemid 23077740)
79. Shen J, Channavajhala P, Seldin DC, Sonenshein GE (2001). Phosphorylation by the protein kinase CK2 promotes calpain-mediated degradation of IkappaBalpha. J Immunol 167, 4919-4925. (Pubitemid 33009721)
80. Shumway SD, Maki M, Miyamoto S (1999). The PEST domain of IkappaBalpha is necessary and sufficient for in vitro degradation by mu-calpain. J Biol Chem 274, 30874-30881. (Pubitemid 129576835)
81. Sorimachi H, Hata S, Ono Y (2011). Impact of genetic insights into calpain biology. J Biochem 150, 23-37.
82. Sun H, Bristow BN, Qu G, Wasserman SA (2002). A heterotrimeric death domain complex in Toll signaling. Proc Natl Acad Sci USA 99, 12871-12876.
83. Sun H, Towb P, Chiem DN, Foster BA, Wasserman SA (2004). Regulated assembly of the Toll signaling complex drives Drosophila dorsoventral patterning. EMBO J 23, 100-110. (Pubitemid 38165751)
84. Tanji T, Yun EY, Ip YT (2010). Heterodimers of NF-kappaB transcription factors DIF and Relish regulate antimicrobial peptide genes in Drosophila. Proc Natl Acad Sci USA 107, 14715-14720.
85. Tauszig-Delamasure S, Bilak H, Capovilla M, Hoffmann JA, Imler JL (2002). Drosophila MyD88 is required for the response to fungal and Gram-positive bacterial infections. Nat Immunol 3, 91-97. (Pubitemid 34065623)
86. Theopold U, Pinter M, Daffre S, Tryselius Y, Friedrich P, Nassel DR, Hultmark D (1995). CalpA, a Drosophila calpain homolog specifically expressed in a small set of nerve, midgut, and blood cells. Mol Cell Biol 15, 824-834.
87. Towb P, Galindo RL, Wasserman SA (1998). Recruitment of Tube and Pelle to signaling sites at the surface of the Drosophila embryo. Development 125, 2443-2450. (Pubitemid 28362404)
88. Whalen AM, Steward R (1993). Dissociation of the dorsal-cactus complex and phosphorylation of the dorsal protein correlate with the nuclear localization of dorsal. J Cell Biol 123, 523-534. (Pubitemid 23324911)
89. Wu LP, Anderson KV (1998). Regulated nuclear import of Rel proteins in the Drosophila immune response. Nature 392, 93-97. (Pubitemid 28150596)
90. Yuan Y, Dopheide SM, Ivanidis C, Salem HH, Jackson SP (1997). Calpain regulation of cytoskeletal signaling complexes in von Willebrand factor-stimulated platelets. Distinct roles for glycoprotein Ib-V-IX and glycoprotein IIb-IIIa (integrin alphaIIbbeta3) in von Willebrand factor-induced signal transduction. J Biol Chem 272, 21847-21854. (Pubitemid 27382801)