The damage threshold hypothesis and the immune strategies of insects

Infection, Genetics and Evolution

Volumn 24, Issue , 2014, Pages 25-33

  Moreno García, Miguel ^a   Condé, Renaud ^a   Bello Bedoy, Rafael ^b   Lanz Mendoza, Humberto ^a  

^a INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^b UNIVERSIDAD AUTÓNOMA DE BAJA CALIFORNIA   (Mexico)

Author keywords

Damage danger; Evolutionary ecology; Immune strategies; Insects; Resistance; Tolerance

Indexed keywords

BACTERIAL VIRULENCE; EVOLUTIONARY ADAPTATION; FUNGAL VIRULENCE; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; INFECTION RESISTANCE; INSECT; MATHEMATICAL MODEL; MIXED INFECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; TISSUE INJURY; ANIMAL; DISEASE RESISTANCE; IMMUNOLOGY;

ANIMALS; DISEASE RESISTANCE; HOST-PATHOGEN INTERACTIONS; IMMUNE TOLERANCE; INSECTS;

EID: 84897907474     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.02.010     Document Type: Review

References (80)

1. Agnew P., Koella J.C. Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proc. R. Soc. Lond. B Biol. Sci. 1997, 264:9-15.
2. Ananthan J., Goldberg A.L., Voellmy R. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 1986, 232:522-524.
3. Anbutsu H., Fukatsu T. Evasion, suppression and tolerance of Drosophila innate immunity by a male-killing Spiroplasma endosymbiont. Insect Mol. Biol. 2010, 19:481-488.
4. Ayres J.S., Schneider D.S. The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol. 2009, 7:e1000150.
5. Ayres J.S., Schneider D.S. Tolerance of infections. Annu. Rev. Immunol. 2012, 30:271-294.
6. Baird N.A., Turnbull D.W., Johnson E.A. Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. J. Biol. Chem. 2006, 281:38675-38681.
7. Bartholomay L.C., Fuchs J.F., Cheng L.-L., Beck E.T., Vizioli J., Lowenberger C., Christensen B.M. Reassessing the role of defensin in the innate immune response of the mosquito, Aedes aegypti. Insect Mol. Biol. 2004, 13:125-132.
8. Bateman A.J. Intra-sexual selection in Drosophila. Heredity 1948, 2:349-368.
9. Bello-Bedoy R., Nunez-Farfan J. The effect of inbreeding on defence against multiple enemies in Datura stramonium. J. Evol. Biol. 2011, 24:518-530.
10. Bello-Bedoy R., Cruz L.L., Núñez-Farfán J. Inbreeding alters a plant-predispersal seed predator interaction. Evol. Ecol. 2011, 25:815-829.
11. Buchon N., Broderick N.A., Chakrabarti S., Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 2009, 23:2333-2344.
12. Buchon N., Broderick N.A., Poidevin M., Pradervand S., Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 2009, 5:200-211.
13. Carval D., Ferriere R. A unified model for the coevolution of resistance, tolerance, and virulence. Evolution 2010, 64:2988-3009.
14. Castillo J., Brown M.R., Strand M.R. Blood feeding and insulin-like peptide 3 stimulate proliferation of hemocytes in the mosquito Aedes aegypti. PLoS Pathog. 2011, 7:e1002274.
15. Choi Y.-J., Fuchs J.F., Mayhew G.F., Yu H.E., Christensen B.M. Tissue-enriched expression profiles in Aedes aegypti identify hemocyte-specific transcriptome responses to infection. Insect Biochem. Mol. Biol. 2012, 42:729-738.
16. Coggins S.A., Estévez-Lao T.Y., Hillyer J.F. Increased survivorship following bacterial infection by the mosquito Aedes aegypti as compared to Anopheles gambiae correlates with increased transcriptional induction of antimicrobial peptides. Dev. Comp. Immunol. 2012, 37:390-401.
17. Cooper E.L. Evolution of immune systems from self/not self to danger to artificial immune systems (AIS). Phys. Life Rev. 2010, 7:55-78.
18. Cunliffe J. Tissue homeostasis and immunity - more on models. Scand. J. Immunol. 2006, 64:172-176.
19. de Roode J.C., Helinski M.E., Anwar M.A., Read A.F. Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am. Nat. 2005, 166:531-542.
20. Eickelberg O., Seebach F., Riordan M., Thulin G., Mann A., Reidy K.H., Van Why S.K., Kashgarian M., Siegel N. Functional activation of heat shock factor and hypoxia-inducible factor in the kidney. J. Am. Soc. Nephrol. 2002, 13:2094-2101.
21. Flegel T., Pasharawipas T. Active viral accommodation: a new concept for crustacean response to viral pathogens. Advances in Shrimp Biotechnology 1998, 245-250. National Center for Genetic Engineering and Biotechnology, Bangkok. T.W. Flegel (Ed.).
22. Flegel T. Hypothesis for heritable, anti-viral immunity in crustaceans and insects. Biol. Direct 2009, 4:32.
23. Fontana M.F., Vance R.E. Two signal models in innate immunity. Immunol. Rev. 2011, 243:26-39.
24. Forbes M.R. On sex differences in optimal immunity. Trends Ecol. Evol. 2007, 22:111-113.
25. Fornoni J., Núñez-Farfán J., Valverde P.L. Evolutionary ecology of tolerance to herbivory: advances and perspectives. Comments Theor. Biol. 2003, 8:643-663.
26. Frank S.A. Models of parasite virulence. Q. Rev. Biol. 1996, 71:37-78.
27. Gallucci S., Matzinger P. Danger signals: SOS to the immune system. Curr. Opin. Immunol. 2001, 13:114-119.
28. Haine E.R., Moret Y., Siva-Jothy M.T., Rolff J. Antimicrobial defense and persistent infection in insects. Science 2008, 322:1257-1259.
29. Hegedus D., Erlandson M., Gillott C., Toprak U. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 2009, 54:285-302.
30. Heil M. Damaged-self recognition as a general strategy for injury detection. Plant Signal. Behav. 2012, 7:576-580.
31. Herrera-Ortiz A., Martínez-Barnetche J., Smit N., Rodriguez M.H., Lanz-Mendoza H. The effect of nitric oxide and hydrogen peroxide in the activation of the systemic immune response of Anopheles albimanus infected with Plasmodium berghei. Dev. Comp. Immunol. 2011, 35:44-50.
32. Hillyer J.F., Schmidt S.L., Christensen B.M. The antibacterial innate immune response by the mosquito Aedes aegypti is mediated by hemocytes and independent of Gram type and pathogenicity. Microbes Infect. 2004, 6:448-459.
33. Hillyer J.F., Schmidt S.L., Fuchs J.F., Boyle J.P., Christensen B.M. Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell. Microbiol. 2005, 7:39-51.
34. Hoffmann J.A. The immune response of Drosophila. Nature 2003, 426:33-38.
35. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20:197-216.
36. Kalske A., Mutikainen P., Muola A., Scheepens J.F., Laukkanen L., Salminen J.P., Leimu R. Simultaneous inbreeding modifies inbreeding depression in a plant-herbivore interaction. Ecol. Lett. 2014, 17:229-238.
37. Khush R.S., Leulier F., Lemaitre B. Pathogen surveillance - the flies have it. Science 2002, 296:273-275.
38. Koella J.C., Lorenz L., Bargielowski I. Microsporidians as evolution-proof agents of malaria control?. Adv. Parasitol. 2009, 68:315-327.
39. Kurtz J. Specific memory within innate immune systems. Trends Immunol. 2005, 26:186-192.
40. Lazzaro B.P., Rolff J. Danger, microbes, and homeostasis. Science 2011, 332:43-44.
41. Lhocine N., Ribeiro P.S., Buchon N., Wepf A., Wilson R., Tenev T., Lemaitre B., Gstaiger M., Meier P., Leulier F. PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 2008, 4:147-158.
42. Ligoxygakis P., Pelte N., Hoffmann J.A., Reichhart J.M. Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 2002, 297:114-116.
43. Luplertlop N., Surasombatpattana P., Patramool S., Dumas E., Wasinpiyamongkol L., Saune L., Hamel R., Bernard E., Sereno D., Thomas F., Piquemal D., Yssel H., Briant L., Missé D. Induction of a peptide with activity against a broad spectrum of pathogens in the Aedes aegypti salivary gland, following infection with dengue virus. PLoS Pathog. 2011, 7:e1001252.
44. Matzinger P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 1994, 12:991-1045.
45. Matzinger P. The danger model: a renewed sense of self. Science 2002, 296:301-305.
46. Matzinger P. Friendly and dangerous signals: is the tissue in control?. Nat. Immunol. 2007, 8:11-13.
47. Matzinger P. The evolution of the danger theory. Expert Rev. Clin. Immunol. 2012, 8:311-317.
48. Matzinger P., Kamala T. Tissue-based class control: the other side of tolerance. Nat. Rev. Immunol. 2011, 11:221-230.
49. McNaughton S.J. Compensatory plant growth as a response to herbivory. Oikos 1983, 40:329-336.
50. Medzhitov R., Schneider D.S., Soares M.P. Disease tolerance as a defense strategy. Science 2012, 335:936-941.
51. Meister M., Lemaitre B., Hoffmann J.A. Antimicrobial peptide defense in Drosophila. Bioessays 1997, 19:1019-1026.
52. Mowlds P., Coates C., Renwick J., Kavanagh K. Dose-dependent cellular and humoral responses in Galleria mellonella larvae following β-glucan inoculation. Microbes Infect. 2010, 12:146-153.
53. Nappi A.J., Ottaviani E. Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 2000, 22:469-480.
54. Núñez-Farfán J., Fornoni J., Valverde P.L. The evolution of resistance and tolerance to herbivores. Annu. Rev. Ecol. Evol. Syst. 2007, 38:541-566.
55. Pal S., St.Leger R.J., Wu L.P. Fungal peptide destruxin a plays a specific role in suppressing the innate immune response in Drosophila melanogaster. J. Biol. Chem. 2007, 282:8969-8977.
56. Pfennig K.S. Evolution of pathogen virulence: the role of variation in host phenotype. Proc. R. Soc. Lond. B Biol. Sci. 2001, 268:755-760.
57. Pradeu T., Cooper E.L. The danger theory: 20years later. Front. Immunol. 2012, 3:287.
58. Råberg L., Graham A.L., Read A.F. Decomposing health: tolerance and resistance to parasites in animals. Philos. Trans. R. Soc. B 2009, 364:37-49.
59. Read A.F., Taylor L.H. The ecology of genetically diverse infections. Science 2001, 292:1099-1102.
60. Read A.F., Graham A.L., Råberg L. Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS Biol. 2008, 6:e1000004.
61. Roy B.A., Kirchner J.W. Evolutionary dynamics of pathogen resistance and tolerance. Evolution 2000, 54:51-63.
62. Rolff J. Bateman's principle and immunity. Proc. R. Soc. Lond. B Biol. Sci. 2002, 269:867-872.
63. Rolff J., Siva-Jothy M.T. Selection on insect immunity in the wild. Proc. R. Soc. Lond. B Biol. Sci. 2004, 271:2157-2160.
64. Schmid-Hempel P. Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. Lond. B Biol. Sci. 2002, 270:357-366.
65. Schmid-Hempel P. Immune defence, parasite evasion strategies and their relevance for 'macroscopic phenomena' such as virulence. Philos. Trans. R. Soc. B 2009, 364:85-98.
66. Schmid-Hempel P., Ebert D. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 2003, 18:27-32.
67. Schmidt O., Theopold U., Strand M. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays 2001, 23:344-351.
68. Schneider D.S., Ayres J.S. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat. Rev. Immunol. 2008, 8:889-895.
69. Schulenburg H., Boehnisch C., Michiels N.K. How do invertebrates generate a highly specific innate immune response?. Mol. Immunol. 2007, 44:3338-3344.
70. Sheldon B.C., Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 1996, 11:317-321.
71. Shinzawa N., Nelson B., Aonuma H., Okado K., Fukumoto S., Miura M., Kanuka H. p38 MAPK-dependent phagocytic encapsulation confers infection tolerance in Drosophila. Cell Host Microbe 2009, 6:244-252.
72. Song M., Pinsky M.R., Kellum J.A. Heat shock factor 1 inhibits nuclear factor-kappaB nuclear binding activity during endotoxin tolerance and heat shock. J. Crit. Care 2008, 23:406-415.
73. Stearns S.C., Ackermann M., Doebeli M., Kaiser M. Experimental evolution of aging, growth, and reproduction in fruitflies. Proc. Natl. Acad. Sci. USA 2000, 97:3309-3313.
74. Stoehr A.M., Kokko H. Sexual dimorphism in immunocompetence: what does life-history theory predict?. Behav. Ecol. 2006, 17:751-756.
75. Stowe K.A., Marquis R.J., Hochwender C.G., Simms E.L. The evolutionary ecology of tolerance to consumer damage. Annu. Rev. Ecol. Syst. 2000, 31:565-595.
76. Svensson E.I., Råberg L. Resistance and tolerance in animal enemy-victim coevolution. Trends Ecol. Evol. 2010, 25:267-274.
77. Tanji T., Hu X., Weber A.N., Ip Y.T. Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol. Cell. Biol. 2007, 27:4578-4588.
78. van Baalen M. Coevolution of recovery ability and virulence. Proc. R. Soc. Lond. B Biol. Sci. 1998, 265:317-325.
79. Van Eden W., Spiering R., Broere F., Zee R. A case of mistaken identity: HSPs are no DAMPs but DAMPERs. Cell Stress Chaperones 2012, 17:281-292.
80. Zhong M., Orosz A., Wu C. Direct sensing of heat and oxidation by Drosophila heat shock transcription factor. Mol. Cell 1998, 2:101-108.