Anopheles stephensi p38 MAPK signaling regulates innate immunity and bioenergetics during Plasmodium falciparum infection

Parasites and Vectors

Volumn 8, Issue 1, 2015, Pages

  Wang, Bo ^a   Pakpour, Nazzy ^a   Napoli, Eleonora ^b   Drexler, Anna ^a   Glennon, Elizabeth K K ^a   Surachetpong, Win ^a   Cheung, Kong ^a   Aguirre, Alejandro ^a   Klyver, John M ^a   Lewis, Edwin E ^b   Eigenheer, Richard ^b   Phinney, Brett S ^b   Giulivi, Cecilia ^b   Luckhart, Shirley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anopheles; Innate immunity; Malaria; MAPK; Mitochondria; Mitogen activated protein kinase; OXPHOS; p38; Plasmodium

Indexed keywords

ANTIBODY; GLUCOSE; LACTIC ACID; MITOGEN ACTIVATED PROTEIN KINASE P38; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; PROTEOME;

ANIMAL CELL; ANOPHELES STEPHENSI; ARTICLE; BIOCHEMICAL ANALYSIS; BIOENERGY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; GLUCOSE METABOLISM; HOST PARASITE INTERACTION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INSECT GENOME; INTESTINE EPITHELIUM; MALARIA CONTROL; MALARIA FALCIPARUM; MIDGUT; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PARASITE TRANSMISSION; PATHOPHYSIOLOGY; PHENOTYPE; PLASMODIUM FALCIPARUM; PROTEIN SYNTHESIS INHIBITION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; ANOPHELES; ENERGY METABOLISM; GENE EXPRESSION PROFILING; IMMUNOLOGY; METABOLISM; SURVIVAL ANALYSIS;

ANOPHELES STEPHENSI; INVERTEBRATA; MAMMALIA; PLASMODIUM FALCIPARUM; VERTEBRATA;

ANIMALS; ANOPHELES; ENERGY METABOLISM; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLASMODIUM FALCIPARUM; PROTEOME; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS;

EID: 84937836069     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-015-1016-x     Document Type: Article

References (104)

1. WHO. World Malaria Report 2014. Geneva: World Health Organization; 2014.
2. Clayton AM, Dong Y, Dimopoulos G. The Anopheles innate immune system in the defense against malaria infection. J Innate Immun. 2014;6(2):169-81. doi: 10.1159/000353602.
3. Whitten MM, Shiao SH, Levashina EA. Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol. 2006;28(4):121-30. doi: 10.1111/j.1365-3024.2006.00804.x.
4. Baton LA, Ranford-Cartwright LC. Ookinete destruction within the mosquito midgut lumen explains Anopheles albimanus refractoriness to Plasmodium falciparum (3D7A) oocyst infection. International J Parasitol. 2012;42(3):249-58. doi: 10.1016/j.ijpara.2011.12.005.
5. Lim J, Gowda DC, Krishnegowda G, Luckhart S. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infect Immun. 2005;73(5):2778-89. doi: 10.1128/IAI.73.5.2778-2789.2005.
6. Luckhart S, Vodovotz Y, Cui L, Rosenberg R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci U S A. 1998;95(10):5700-5.
7. Pakpour N, Camp L, Smithers HM, Wang B, Tu Z, Nadler SA, et al. Protein kinase C-dependent signaling controls the midgut epithelial barrier to malaria parasite infection in anopheline mosquitoes. PloS One. 2013;8(10):e76535.
8. Peterson TM, Gow AJ, Luckhart S. Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Rad Biol Med. 2007;42(1):132-42. doi: 10.1016/j.freeradbiomed.2006.10.037.
9. Surachetpong W, Singh N, Cheung KW, Luckhart S. MAPK ERK signaling regulates the TGF-beta1-dependent mosquito response to Plasmodium falciparum. PLoS Pathog. 2009;5(4):e1000366. doi: 10.1371/journal.ppat.1000366.
10. Blandin S, Moita LF, Kocher T, Wilm M, Kafatos FC, Levashina EA. Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep. 2002;3(9):852-6. doi: 10.1093/embo-reports/kvf180.
11. Povelones M, Waterhouse RM, Kafatos FC, Christophides GK. Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science. 2009;324(5924):258-61. doi: 10.1126/science.1171400.
12. Mitri C, Jacques JC, Thiery I, Riehle MM, Xu J, Bischoff E, et al. Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog. 2009;5(9):e1000576. doi: 10.1371/journal.ppat.1000576.
13. Riehle MM, Markianos K, Niare O, Xu J, Li J, Toure AM, et al. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science. 2006;312(5773):577-9. doi: 10.1126/science.1124153.
14. Osta MA, Christophides GK, Kafatos FC. Effects of mosquito genes on Plasmodium development. Science. 2004;303(5666):2030-2. doi: 10.1126/science.1091789.
15. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2006;2(6):e52. doi: 10.1371/journal.ppat.0020052.
16. Vlachou D, Zimmermann T, Cantera R, Janse CJ, Waters AP, Kafatos FC. Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol. 2004;6(7):671-85. doi: 10.1111/j.1462-5822.2004.00394.x.
17. Dong C, Davis RJ, Flavell RA. MAP kinases in the immune response. Annual Rev Immunol. 2002;20:55-72. doi: 10.1146/annurev.immunol.20.091301.131133.
18. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124(4):783-801. doi: 10.1016/j.cell.2006.02.015.
19. Chen J, Xie C, Tian L, Hong L, Wu X, Han J. Participation of the p38 pathway in Drosophila host defense against pathogenic bacteria and fungi. Proc Natl Acad Sci U S A. 2010;107(48):20774-9. doi: 10.1073/pnas.1009223107.
20. Han ZS, Enslen H, Hu X, Meng X, Wu IH, Barrett T, et al. A conserved p38 mitogen-activated protein kinase pathway regulates Drosophila immunity gene expression. Molec Cell Biol. 1998;18(6):3527-39.
21. Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, Inoue H, et al. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science. 2002;297(5581):623-6. doi: 10.1126/science.1073759.
22. Ono K, Han J. The p38 signal transduction pathway: activation and function. Cell Signal. 2000;12(1):1-13.
23. Chen-Chih Wu R, Shaio MF, Cho WL. A p38 MAP kinase regulates the expression of the Aedes aegypti defensin gene in mosquito cells. Insect Molec Biol. 2007;16(4):389-99. doi: 10.1111/j.1365-2583.2007.00734.x.
24. Cancino-Rodezno A, Alexander C, Villasenor R, Pacheco S, Porta H, Pauchet Y, et al. The mitogen-activated protein kinase p38 is involved in insect defense against Cry toxins from Bacillus thuringiensis. Insect Biochem Mol Biol. 2010;40(1):58-63. doi: 10.1016/j.ibmb.2009.12.010.
25. Moon AE, Walker AJ, Goodbourn S. Regulation of transcription of the Aedes albopictus cecropin A1 gene: A role for p38 mitogen-activated protein kinase. Insect Biochem Mol Biol. 2011;41(8):628-36. doi: 10.1016/j.ibmb.2011.04.001.
26. Ha EM, Lee KA, Seo YY, Kim SH, Lim JH, Oh BH, et al. Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nat Immunol. 2009;10(9):949-57. doi: 10.1038/ni.1765.
27. Park JS, Kim YS, Yoo MA. The role of p38b MAPK in age-related modulation of intestinal stem cell proliferation and differentiation in Drosophila. Aging (Albany NY). 2009;1(7):637-51.
28. Park JS, Kim YS, Kim JG, Lee SH, Park SY, Yamaguchi M, et al. Regulation of the Drosophila p38b gene by transcription factor DREF in the adult midgut. Biochim Biophys Acta. 2010;1799(7):510-9. doi: 10.1016/j.bbagrm.2010.03.001.
29. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2006;2(11):e183. doi: 10.1371/journal.pgen.0020183.
30. Hoeven R, McCallum KC, Cruz MR, Garsin DA. Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog. 2011;7(12):e1002453. doi: 10.1371/journal.ppat.1002453.
31. Horton AA, Wang B, Camp L, Price MS, Arshi A, Nagy M, et al. The mitogen-activated protein kinome from Anopheles gambiae: identification, phylogeny and functional characterization of the ERK, JNK and p38 MAP kinases. BMC Genomics. 2011;12:574. doi: 10.1186/1471-2164-12-574.
32. Vodovotz YAN, Miskov-Zivanov N, Buliga M, Zamora R, Ermentrout B, Constantine GM, et al. Modeling Host-Vector-Pathogen Immuno- inflammatory Interactions in Malaria. In: Vodovotz YAG, editor. Complex Systems and Computational Biology Approaches to Acute Inflammation. New York: Springer Science+Business Media; 2013. p. 291.
33. Matsuzawa A, Ichijo H. Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim Biophys Acta. 2008;1780(11):1325-36. doi: 10.1016/j.bbagen.2007.12.011.
34. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev. 2001;81(2):807-69.
35. Surachetpong W, Pakpour N, Cheung KW, Luckhart S. Reactive oxygen species-dependent cell signaling regulates the mosquito immune response to Plasmodium falciparum. Antiox Redox Signal. 2011;14(6):943-55. doi: 10.1089/ars.2010.3401.
36. Son Y, Kim S, Chung HT, Pae HO. Reactive oxygen species in the activation of MAP kinases. Methods Enzymol. 2013;528:27-48. doi: 10.1016/B978-0-12-405881-1.00002-1.
37. Shinzawa N, Nelson B, Aonuma H, Okado K, Fukumoto S, Miura M, et al. p38 MAPK-dependent phagocytic encapsulation confers infection tolerance in Drosophila. Cell Host Microbe. 2009;6(3):244-52. doi: 10.1016/j.chom.2009.07.010.
38. Vrailas-Mortimer A, del Rivero T, Mukherjee S, Nag S, Gaitanidis A, Kadas D, et al. A muscle-specific p38 MAPK/Mef2/MnSOD pathway regulates stress, motor function, and life span in Drosophila. Dev Cell. 2011;21(4):783-95. doi: 10.1016/j.devcel.2011.09.002.
39. Gostner JM, Becker K, Fuchs D, Sucher R. Redox regulation of the immune response. Redox Rep. 2013;18(3):88-94. doi: 10.1179/1351000213Y.0000000044.
40. Gutierrez-Uzquiza A, Arechederra M, Bragado P, Aguirre-Ghiso JA, Porras A. p38alpha mediates cell survival in response to oxidative stress via induction of antioxidant genes: effect on the p70S6K pathway. J Biol Chem. 2012;287(4):2632-42. doi: 10.1074/jbc.M111.323709.
41. Molina-Cruz A, DeJong RJ, Charles B, Gupta L, Kumar S, Jaramillo-Gutierrez G, et al. Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem. 2008;283(6):3217-23. doi: 10.1074/jbc.M705873200.
42. Lanz-Mendoza H, Hernandez-Martinez S, Ku-Lopez M, Rodriguez Mdel C, Herrera-Ortiz A, Rodriguez MH. Superoxide anion in Anopheles albimanus hemolymph and midgut is toxic to Plasmodium berghei ookinetes. J Parasitol. 2002;88(4):702-6. doi:10.1645/0022-3395(2002)088[0702:SAIAAH]2.0.CO;2.
43. Brune B, Dehne N, Grossmann N, Jung M, Namgaladze D, Schmid T, et al. Redox control of inflammation in macrophages. Antioxid Redox Signal. 2013;19(6):595-637. doi: 10.1089/ars.2012.4785.
44. Gloire G, Legrand-Poels S, Piette J. NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol. 2006;72(11):1493-505. doi: 10.1016/j.bcp.2006.04.011.
45. Shaw G, Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986;46(5):659-67.
46. Shyu AB, Greenberg ME, Belasco JG. The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev. 1989;3(1):60-72.
47. Tiedje C, Ronkina N, Tehrani M, Dhamija S, Laass K, Holtmann H, et al. The p38/MK2-driven exchange between tristetraprolin and HuR regulates AU-rich element-dependent translation. PLoS Genet. 2012;8(9):e1002977. doi: 10.1371/journal.pgen.1002977.
48. Winzen R, Kracht M, Ritter B, Wilhelm A, Chen CY, Shyu AB, et al. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 1999;18(18):4969-80. doi: 10.1093/emboj/18.18.4969.
49. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1(6):361-70. doi: 10.1016/j.cmet.2005.05.004.
50. Lai L, Leone TC, Zechner C, Schaeffer PJ, Kelly SM, Flanagan DP, et al. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev. 2008;22(14):1948-61. doi: 10.1101/gad.1661708.
51. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92(6):829-39.
52. Huss JM, Kopp RP, Kelly DP. Peroxisome proliferator-activated receptor coactivator-1alpha (PGC-1alpha) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-alpha and -gamma. Identification of novel leucine-rich interaction motif within PGC-1alpha. J Biol Chem. 2002;277(43):40265-74. doi: 10.1074/jbc.M206324200.
53. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115-24. doi: 10.1016/S0092-8674(00)80611-X.
54. Chambers KT, Chen Z, Lai L, Leone TC, Towle HC, Kralli A, et al. PGC-1beta and ChREBP partner to cooperatively regulate hepatic lipogenesis in a glucose concentration-dependent manner. Molec Metab. 2013;2(3):194-204. doi: 10.1016/j.molmet.2013.05.001.
55. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, Rhee J, et al. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature. 2001;413(6852):131-8. doi: 10.1038/35093050.
56. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, et al. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature. 2001;413(6852):179-83. doi: 10.1038/35093131.
57. Lin J, Yang R, Tarr PT, Wu PH, Handschin C, Li S, et al. Hyperlipidemic effects of dietary saturated fats mediated through PGC-1beta coactivation of SREBP. Cell. 2005;120(2):261-73. doi: 10.1016/j.cell.2004.11.043.
58. Sonoda J, Laganiere J, Mehl IR, Barish GD, Chong LW, Li X, et al. Nuclear receptor ERR alpha and coactivator PGC-1 beta are effectors of IFN-gamma-induced host defense. Genes Dev. 2007;21(15):1909-20. doi: 10.1101/gad.1553007.
59. Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, et al. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 2006;4(1):13-24. doi: 10.1016/j.cmet.2006.05.011.
60. Tiefenbock SK, Baltzer C, Egli NA, Frei C. The Drosophila PGC-1 homologue Spargel coordinates mitochondrial activity to insulin signalling. EMBO J. 2010;29(1):171-83. doi: 10.1038/emboj.2009.330.
61. Rera M, Bahadorani S, Cho J, Koehler CL, Ulgherait M, Hur JH, et al. Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metab. 2011;14(5):623-34. doi: 10.1016/j.cmet.2011.09.013.
62. Mukherjee S, Duttaroy A. Spargel/dPGC-1 is a new downstream effector in the insulin-TOR signaling pathway in Drosophila. Genetics. 2013;195(2):433-41. doi: 10.1534/genetics.113.154583.
63. Luckhart S, Giulivi C, Drexler AL, Antonova-Koch Y, Sakaguchi D, Napoli E, et al. Sustained activation of Akt elicits mitochondrial dysfunction to block Plasmodium falciparum infection in the mosquito host. PLoS Pathog. 2013;9(2):e1003180. doi: 10.1371/journal.ppat.1003180.
64. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Molecular Biol. 1990;215(3):403-10. doi: 10.1016/S0022-2836(05)80360-2.
65. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nuc Acids Res. 1984;12(2):857-72.
66. Pakpour N, Corby-Harris V, Green GP, Smithers HM, Cheung KW, Riehle MA, et al. Ingested human insulin inhibits the mosquito NF-kappaB-dependent immune response to Plasmodium falciparum. Infect Immun. 2012;80(6):2141-9. doi: 10.1128/IAI.00024-12.
67. Lambros C, Vanderberg JP. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol. 1979;65(3):418-20.
68. Hauck ES, Antonova-Koch Y, Drexler A, Pietri J, Pakpour N, Liu D, et al. Overexpression of phosphatase and tensin homolog improves fitness and decreases Plasmodium falciparum development in Anopheles stephensi. Microbes Infect. 2013;15(12):775-87. doi: 10.1016/j.micinf.2013.05.006.
69. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002;74(20):5383-92.
70. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75(17):4646-58.
71. Tabb DL. What's driving false discovery rates? J Proteome Res. 2008;7(1):45-6. doi: 10.1021/pr700728t.
72. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Meth. 2012;9(7):671-5.
73. Beutler E. Red cell metabolism: a manual of biochemical methods. 3rd ed. Orlando, FL: Grune & Stratton; 1984.
74. Giulivi C, Zhang YF, Omanska-Klusek A, Ross-Inta C, Wong S, Hertz-Picciotto I, et al. Mitochondrial dysfunction in autism. JAMA. 2010;304(21):2389-96. doi: 10.1001/jama.2010.1706.
75. Zhang J, Shen B, Lin A. Novel strategies for inhibition of the p38 MAPK pathway. Trends Pharmacol Sci. 2007;28(6):286-95. doi: 10.1016/j.tips.2007.04.008.
76. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, et al. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 1995;364(2):229-33.
77. Kuma Y, Sabio G, Bain J, Shpiro N, Marquez R, Cuenda A. BIRB796 inhibits all p38 MAPK isoforms in vitro and in vivo. J Biol Chem. 2005;280(20):19472-9. doi: 10.1074/jbc.M414221200.
78. Pargellis C, Tong L, Churchill L, Cirillo PF, Gilmore T, Graham AG, et al. Inhibition of p38 MAP kinase by utilizing a novel allosteric binding site. Nat Struc Biol. 2002;9(4):268-72. doi: 10.1038/nsb770.
79. Wilson KP, Fitzgibbon MJ, Caron PR, Griffith JP, Chen W, McCaffrey PG, et al. Crystal structure of p38 mitogen-activated protein kinase. J Biol Chem. 1996;271(44):27696-700.
80. Wood CD, Thornton TM, Sabio G, Davis RA, Rincon M. Nuclear localization of p38 MAPK in response to DNA damage. Intl J Biol Sci. 2009;5(5):428-37.
81. Dorin-Semblat D, Quashie N, Halbert J, Sicard A, Doerig C, Peat E, et al. Functional characterization of both MAP kinases of the human malaria parasite Plasmodium falciparum by reverse genetics. Molec Microbiol. 2007;65(5):1170-80. doi: 10.1111/j.1365-2958.2007.05859.x.
82. Brumlik MJ, Nkhoma S, Kious MJ, Thompson 3rd GR, Patterson TF, Siekierka JJ, et al. Human p38 mitogen-activated protein kinase inhibitor drugs inhibit Plasmodium falciparum replication. Exp Parasitol. 2011;128(2):170-5. doi: 10.1016/j.exppara.2011.02.016.
83. Ashwell JD. The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nat Rev Immunol. 2006;6(7):532-40. doi: 10.1038/nri1865.
84. Roux PP, Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Molec Biol Rev. 2004;68(2):320-44. doi: 10.1128/MMBR.68.2.320-344.2004.
85. Figueira TR, Barros MH, Camargo AA, Castilho RF, Ferreira JC, Kowaltowski AJ, et al. Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antiox Redox Signal. 2013;18(16):2029-74. doi: 10.1089/ars.2012.4729.
86. Ockenhouse CF, Shear HL. Oxidative killing of the intraerythrocytic malaria parasite Plasmodium yoelii by activated macrophages. J Immunol. 1984;132(1):424-31.
87. Dockrell HM, Playfair JH. Killing of blood-stage murine malaria parasites by hydrogen peroxide. Infect Immun. 1983;39(1):456-9.
88. Kumar S, Christophides GK, Cantera R, Charles B, Han YS, Meister S, et al. The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci U S A. 2003;100(24):14139-44. doi: 10.1073/pnas.2036262100.
89. Drexler AL, Pietri JE, Pakpour N, Hauck E, Wang B, Glennon EK, et al. Human IGF1 regulates midgut oxidative stress and epithelial homeostasis to balance lifespan and Plasmodium falciparum resistance in Anopheles stephensi. PLoS Pathog. 2014;10(6):e1004231. doi: 10.1371/journal.ppat.1004231.
90. Venigalla RK, Turner M. RNA-binding proteins as a point of convergence of the PI3K and p38 MAPK pathways. Front Immunol. 2012;3:398. doi: 10.3389/fimmu.2012.00398.
91. Arthur JS, Ley SC. Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol. 2013;13(9):679-92. doi: 10.1038/nri3495.
92. Fernandez-Marcos PJ, Auwerx J. Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr. 2011;93(4):884S-90. doi: 10.3945/ajcn.110.001917.
93. Puigserver P, Rhee J, Lin J, Wu Z, Yoon JC, Zhang CY, et al. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Molec Cell. 2001;8(5):971-82.
94. Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev. 2003;24(1):78-90.
95. Xiong Y, Collins QF, An J, Lupo Jr E, Liu HY, Liu D, et al. p38 mitogen-activated protein kinase plays an inhibitory role in hepatic lipogenesis. J Biol Chem. 2007;282(7):4975-82. doi: 10.1074/jbc.M606742200.
96. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 2006;127(2):397-408. doi: 10.1016/j.cell.2006.09.024.
97. Dong Y, Manfredini F, Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009;5(5):e1000423. doi: 10.1371/journal.ppat.1000423.
98. Gusmao DS, Santos AV, Marini DC, Bacci Jr M, Berbert-Molina MA, Lemos FJ. Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Trop. 2010;115(3):275-81. doi: 10.1016/j.actatropica.2010.04.011.
99. Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am J Trop Med Hyg. 1996;54(2):214-8.
100. Wang Y, Gilbreath 3rd TM, Kukutla P, Yan G, Xu J. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PloS One. 2011;6(9):e24767. doi: 10.1371/journal.pone.0024767.
101. Caro HN, Sheikh NA, Taverne J, Playfair JH, Rademacher TW. Structural similarities among malaria toxins insulin second messengers, and bacterial endotoxin. Infect Immun. 1996;64(8):3438-41.
102. Mead EA, Li M, Tu Z, Zhu J. Translational regulation of Anopheles gambiae mRNAs in the midgut during Plasmodium falciparum infection. BMC Genomics. 2012;13:366. doi: 10.1186/1471-2164-13-366.
103. Zhu G, Zhong D, Cao J, Zhou H, Li J, Liu Y, et al. Transcriptome profiling of pyrethroid resistant and susceptible mosquitoes in the malaria vector, Anopheles sinensis. BMC Genomics. 2014;15:448. doi: 10.1186/1471-2164-15-448.
104. Fossog Tene B, Poupardin R, Costantini C, Awono-Ambene P, Wondji CS, Ranson H, et al. Resistance to DDT in an urban setting: common mechanisms implicated in both M and S forms of Anopheles gambiae in the city of Yaounde Cameroon. PloS One. 2013;8(4):e61408. doi: 10.1371/journal.pone.0061408.