Protein Kinase C-Dependent Signaling Controls the Midgut Epithelial Barrier to Malaria Parasite Infection in Anopheline Mosquitoes

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Pakpour, Nazzy ^a   Camp, Lauren ^b   Smithers, Hannah M ^a   Wang, Bo ^a   Tu, Zhijian ^c   Nadler, Steven A ^b   Luckhart, Shirley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN KINASE C;

ANOPHELES; ANOPHELES GAMBIAE; ANOPHELES STEPHENSI; ARTICLE; BLOOD FEEDING; ENZYME INHIBITION; FEEDING; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE SEQUENCE; GENETIC CONSERVATION; HOST PARASITE INTERACTION; IN VITRO STUDY; INSECT CELL; INTESTINE EPITHELIUM; MALARIA; MIDGUT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PKC GENE; PKCDELTA GENE; PKCEPSILON GENE; PKCZETA GENE; PKD GENE; PKN GENE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; ANOPHELES; BAYES THEOREM; DIGESTIVE SYSTEM; ENZYME ACTIVATION; EPITHELIUM; LIPOPOLYSACCHARIDES; MALARIA; MULTIGENE FAMILY; NF-KAPPA B; PARASITES; PHYLOGENY; PLASMODIUM FALCIPARUM; PROMOTER REGIONS, GENETIC; PROTEIN KINASE C; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION;

EID: 84885393900     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076535     Document Type: Article

References (88)

1. Rosse C, Linch M, Kermorgant S, Cameron AJ, Boeckeler K, et al. (2010) PKC and the control of localized signal dynamics. Nat Rev Mol Cell Biol 11: 103-112.
2. Shieh BH, Parker L, Popescu D, (2002) Protein kinase C (PKC) isoforms in Drosophila. J Biochem 132: 523-527.
3. Maier D, Hausser A, Nagel AC, Link G, Kugler SJ, et al. (2006) Drosophila protein kinase D is broadly expressed and a fraction localizes to the Golgi compartment. Gene Expr Patterns 6: 849-856.
4. Rozengurt E, Rey O, Waldron RT, (2005) Protein kinase D signaling. J Biol Chem 280: 13205-13208.
5. World Health Organization. (2012) World malaria report. Geneva, Switzerland: World Health Organization. pp. v.
6. Dawes EJ, Churcher TS, Zhuang S, Sinden RE, Basanez MG, (2009) Anopheles mortality is both age- and Plasmodium-density dependent: implications for malaria transmission. Malar J 8: 228.
7. Vlachou D, Zimmermann T, Cantera R, Janse CJ, Waters AP, et al. (2004) Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol 6: 671-685.
8. Billingsley PF, (1990) The Midgut Ultrastructure of Hematophagous Insects. Annual Review of Entomology 35: 219-248.
9. Beyenbach KW, (2012) A dynamic paracellular pathway serves diuresis in mosquito Malpighian tubules. Ann N Y Acad Sci 1258: 166-176.
10. Andreeva AY, Krause E, Muller EC, Blasig IE, Utepbergenov DI, (2001) Protein kinase C regulates the phosphorylation and cellular localization of occludin. J Biol Chem 276: 38480-38486.
11. Stuart RO, Nigam SK, (1995) Regulated assembly of tight junctions by protein kinase C. Proc Natl Acad Sci U S A. 92: 6072-6076.
12. Furuse M, Tsukita S, (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16: 181-188.
13. Sotillos S, Diaz-Meco MT, Caminero E, Moscat J, Campuzano S, (2004) DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. J Cell Biol 166: 549-557.
14. Meister S, Kanzok SM, Zheng XL, Luna C, Li TR, et al. (2005) Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 102: 11420-11425.
15. Gilmore TD, Wolenski FS, (2012) NF-kappaB: where did it come from and why? Immunol Rev 246: 14-35.
16. Garver LS, Dong Y, Dimopoulos G, (2009) Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 5: e1000335.
17. Moscat J, Rennert P, Diaz-Meco MT, (2006) PKCzeta at the crossroad of NF-kappaB and Jak1/Stat6 signaling pathways. Cell Death Differ 13: 702-711.
18. Coudronniere N, Villalba M, Englund N, Altman A, (2000) NF-kappa B activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-theta. Proc Natl Acad Sci U S A 97: 3394-3399.
19. Huang X, Chen LY, Doerner AM, Pan WW, Smith L, et al. (2009) An atypical protein kinase C (PKC zeta) plays a critical role in lipopolysaccharide-activated NF-kappa B in human peripheral blood monocytes and macrophages. J Immunol 182: 5810-5815.
20. Avila A, Silverman N, Diaz-Meco MT, Moscat J, (2002) The Drosophila atypical protein kinase C-ref(2)p complex constitutes a conserved module for signaling in the toll pathway. Mol Cell Biol 22: 8787-8795.
21. Wullaert A, Bonnet MC, Pasparakis M, (2011) NF-kappaB in the regulation of epithelial homeostasis and inflammation. Cell Res 21: 146-158.
22. Aveleira CA, Lin CM, Abcouwer SF, Ambrosio AF, Antonetti DA, (2010) TNF-alpha signals through PKCzeta/NF-kappaB to alter the tight junction complex and increase retinal endothelial cell permeability. Diabetes 59: 2872-2882.
23. Musacchio A, Gibson T, Rice P, Thompson J, Saraste M, (1993) The PH domain: a common piece in the structural patchwork of signalling proteins. Trends Biochem Sci 18: 343-348.
24. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
25. Castresana J, (2000) Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. Molecular Biology and Evolution 17: 540-552.
26. Baker DA, Nolan T, Fischer B, Pinder A, Crisanti A, et al. (2011) A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae. BMC Genomics 12: 296.
27. Marinotti O, Nguyen QK, Calvo E, James AA, Ribeiro JM, (2005) Microarray analysis of genes showing variable expression following a blood meal in Anopheles gambiae. Insect Mol Biol 14: 365-373.
28. Vlachou D, Schlegelmilch T, Christophides GK, Kafatos FC, (2005) Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr Biol 15: 1185-1195.
29. Ward P, Equinet L, Packer J, Doerig C, (2004) Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5: 79.
30. Asehnoune K, Strassheim D, Mitra S, Yeol Kim J, Abraham E, (2005) Involvement of PKCalpha/beta in TLR4 and TLR2 dependent activation of NF-kappaB. Cell Signal 17: 385-394.
31. Valledor AF, Xaus J, Comalada M, Soler C, Celada A, (2000) Protein kinase C epsilon is required for the induction of mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J Immunol 164: 29-37.
32. Loegering DJ, Lennartz MR, (2011) Protein kinase C and toll-like receptor signaling. Enzyme Res 2011: 537821.
33. Pakpour N, Corby-Harris V, Green GP, Smithers HM, Cheung KW, et al. (2012) Ingested Human Insulin Inhibits the Mosquito NF-kappaB-Dependent Immune Response to Plasmodium falciparum. Infect Immun 80: 2141-2149.
34. Gupta L, Molina-Cruz A, Kumar S, Rodrigues J, Dixit R, et al. (2009) The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe 5: 498-507.
35. Luckhart S, Rosenberg R, (1999) Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene 232: 25-34.
36. Luckhart S, Vodovotz Y, Cui L, Rosenberg R, (1998) The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci U S A 95: 5700-5705.
37. Cohuet A, Osta MA, Morlais I, Awono-Ambene PH, Michel K, et al. (2006) Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Rep 7: 1285-1289.
38. Blandin S, Moita LF, Kocher T, Wilm M, Kafatos FC, et al. (2002) Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep 3: 852-856.
39. Riehle MM, Markianos K, Niare O, Xu J, Li J, et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577-579.
40. Jain S, Suzuki T, Seth A, Samak G, Rao R, (2011) Protein kinase Czeta phosphorylates occludin and promotes assembly of epithelial tight junctions. Biochem J 437: 289-299.
41. Elias BC, Suzuki T, Seth A, Giorgianni F, Kale G, et al. (2009) Phosphorylation of Tyr-398 and Tyr-402 in occludin prevents its interaction with ZO-1 and destabilizes its assembly at the tight junctions. J Biol Chem 284: 1559-1569.
42. Turner JR, (2006) Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 169: 1901-1909.
43. Clayburgh DR, Shen L, Turner JR, (2004) A porous defense: the leaky epithelial barrier in intestinal disease. Lab Invest 84: 282-291.
44. Koyanagi M, Ono K, Suga H, Iwabe N, Miyata T, (1998) Phospholipase C cDNAs from sponge and hydra: antiquity of genes involved in the inositol phospholipid signaling pathway. FEBS Lett 439: 66-70.
45. Bradham CA, Foltz KR, Beane WS, Arnone MI, Rizzo F, et al. (2006) The sea urchin kinome: a first look. Dev Biol 300: 180-193.
46. Bahia D, Avelar L, Mortara RA, Khayath N, Yan Y, et al. (2006) SmPKC1, a new protein kinase C identified in the platyhelminth parasite Schistosoma mansoni. Biochem Biophys Res Commun 345: 1138-1148.
47. Kofler K, Erdel M, Utermann G, Baier G, (2002) Molecular genetics and structural genomics of the human protein kinase C gene module. Genome Biol 3: RESEARCH0014.
48. Nishizuka Y, (1988) The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334: 661-665.
49. Disatnik MH, Buraggi G, Mochly-Rosen D, (1994) Localization of protein kinase C isozymes in cardiac myocytes. Exp Cell Res 210: 287-297.
50. Akman-Anderson L, Olivier M, Luckhart S, (2007) Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infect Immun 75: 4012-4019.
51. Newton AC, (1997) Regulation of protein kinase C. Curr Opin Cell Biol. 9: 161-167.
52. Nelson TJ, Sun MK, Hongpaisan J, Alkon DL, (2008) Insulin, PKC signaling pathways and synaptic remodeling during memory storage and neuronal repair. Eur J Pharmacol 585: 76-87.
53. Clerk A, Sugden PH, (2001) Untangling the Web: specific signaling from PKC isoforms to MAPK cascades. Circ Res 89: 847-849.
54. Marinissen MJ, Gutkind JS, (2001) G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol Sci 22: 368-376.
55. Oeckinghaus A, Hayden MS, Ghosh S, (2011) Crosstalk in NF-kappaB signaling pathways. Nat Immunol 12: 695-708.
56. Graca-Souza AV, Maya-Monteiro C, Paiva-Silva GO, Braz GR, Paes MC, et al. (2006) Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem Mol Biol 36: 322-335.
57. Droge W, (2002) Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95.
58. Gopalakrishna R, Jaken S, (2000) Protein kinase C signaling and oxidative stress. Free Radic Biol Med 28: 1349-1361.
59. Oliveira JH, Goncalves RL, Lara FA, Dias FA, Gandara AC, et al. (2011) Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog 7: e1001320.
60. Cirimotich CM, Ramirez JL, Dimopoulos G, (2011) Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10: 307-310.
61. Dong Y, Manfredini F, Dimopoulos G, (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5: e1000423.
62. Meister S, Agianian B, Turlure F, Relogio A, Morlais I, et al. (2009) Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 5: e1000542.
63. Rao R, (2009) Occludin phosphorylation in regulation of epithelial tight junctions. Ann N Y Acad Sci 1165: 62-68.
64. Scott KG, Meddings JB, Kirk DR, Lees-Miller SP, Buret AG, (2002) Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology 123: 1179-1190.
65. Zolotarevsky Y, Hecht G, Koutsouris A, Gonzalez DE, Quan C, et al. (2002) A membrane-permeant peptide that inhibits MLC kinase restores barrier function in in vitro models of intestinal disease. Gastroenterology 123: 163-172.
66. Canning EU, Sinden RE, (1973) The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67: 29-40.
67. Han YS, Thompson J, Kafatos FC, Barillas-Mury C, (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J 19: 6030-6040.
68. Yu D, Marchiando AM, Weber CR, Raleigh DR, Wang Y, et al. (2010) MLCK-dependent exchange and actin binding region-dependent anchoring of ZO-1 regulate tight junction barrier function. Proc Natl Acad Sci U S A 107: 8237-8241.
69. Baier G, Wagner J, (2009) PKC inhibitors: potential in T cell-dependent immune diseases. Curr Opin Cell Biol 21: 262-267.
70. Cohen P, (2002) Protein kinases-the major drug targets of the twenty-first century? Nat Rev Drug Discov 1: 309-315.
71. Friman S, Arns W, Nashan B, Vincenti F, Banas B, et al. (2011) Sotrastaurin, a novel small molecule inhibiting protein-kinase C: randomized phase II study in renal transplant recipients. Am J Transplant 11: 1444-1455.
72. Yamashita K, Todo S, (2012) Sotrastaurin, a new selective protein kinase C inhibitor, on the way. Transplantation 93: 146-147.
73. Millholland MG, Mishra S, Dupont CD, Love MS, Patel B, et al. (2013) A host GPCR signaling network required for the cytolysis of infected cells facilitates release of apicomplexan parasites. Cell Host Microbe 13: 15-28.
74. Kovarik JM, Neuhaus P, Cillo U, Weber M, Stitah S, et al. (2011) Sotrastaurin single-dose pharmacokinetics in de novo liver transplant recipients. Transpl Int 24: 276-283.
75. Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, et al. (2012) The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. PLoS Med 9: e1001169.
76. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
77. Eddy SR, (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
78. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-222.
79. Kozak M, (1984) Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res 12: 857-872.
80. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
81. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
82. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees; 2010 14-14 Nov. 2010: 1-8.
83. Surachetpong W, Pakpour N, Cheung KW, Luckhart S, (2011) Reactive oxygen species-dependent cell signaling regulates the mosquito immune response to Plasmodium falciparum. Antioxid Redox Signal 14: 943-955.
84. Lambros C, Vanderberg JP, (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
85. Dong Y, Das S, Cirimotich C, Souza-Neto JA, McLean KJ, et al. (2011) Engineered anopheles immunity to Plasmodium infection. PLoS Pathog 7: e1002458.
86. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
87. Fallon AM, Stollar V, (1987) The biochemistry and genetics of mosquito cells in culture. Adv Cell Culture 5: 97-137.
88. Hauck ES, Antonova-Koch Y, Drexler A, Pietri J, Pakpour N, et al. (2013) Overexpression of phosphatase and tensin homolog improves fitness and decreases Plasmodium falciparum development in Anopheles stephensi. Microbes Infect.