Hormonal regulation of energy metabolism in insects as a driving force for performance

Integrative and Comparative Biology

Volumn 49, Issue 4, 2009, Pages 380-392

  Lorenz, Matthias W ^a   Gäde, Gerd ^b  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

HEXAPODA;

EID: 70349449682     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/icp019     Document Type: Article

References (105)

1. Anand AN, Lorenz MW. 2008. Age-dependent changes of fat body stores and the regulation of fat body lipid synthesis and mobilisation by adipokinetic hormone in the last larval instar of the cricket, Gryllus bimaculatus. J Insect Physiol 54:1404-1412
2. Arrese EL, Canavoso LE, Jouni ZE, Pennington JE, Tsuchida K, Wells MA. 2001. Lipid storage and mobilization in insects: current status and future directions. Insect Biochem Mol Biol 31:7-17
3. Ashhurst DE, Luke BM. 1968. Lipid inclusions in the flight muscles of belostomatid water-bugs. Z Zellforsch Mikrosk Anat 92:270-274
4. Auerswald L, Gäde G. 1999a. Effects of metabolic neuropeptides from insect corpora cardiaca on proline metabolism of the African fruit beetle, Pachnoda sinuata. J Insect Physiol 45:535-543
5. Auerswald L, Gäde G. 1999b. The fate of proline in the African fruit beetle Pachnoda sinuata. Insect Biochem Mol Biol 29:687-700
6. Auerswald L, Gäde G. 2000a. Cyclic AMP mediates the elevation of proline by AKH peptides in the cetoniid beetle, Pachnoda sinuata. Biochim Biophys Acta 1495: 78-89
7. Auerswald L, Gäde G. 2000b. Metabolic changes in the African fruit beetle, Pachnoda sinuata, during starvation. J Insect Physiol 46:343-351
8. Auerswald L, Gäde G. 2001a. The role of calcium in the activation of glycogen phosphorylase in the fat body of the fruit beetle, Pachnoda sinuata, by hypertrehalosaemic hormone. Biochim Biophys Acta 1499:199-208 (Pubitemid 32332763)
9. Auerswald L, Gäde G. 2001b. Hormonal stimulation of proline synthesis in the fat body of the fruit beetle, Pachnoda sinuata, is calcium dependent. Insect Biochem Mol Biol 32:23-32
10. Auerswald L, Gäde G. 2002. The role of Ins(1,4,5)P3 in signal transduction of the metabolic neuropeptide Mem-CC in the cetoniid beetle, Pachnoda sinuata. Insect Biochem Mol Biol 32:1793-1803
11. Auerswald L, Schneider P, Gäde G. 1998a. Proline powers pre-flight warm-up in the African fruit beetle Pachnoda sinuata (Cetoniinae). J Exp Biol 201:1651-1657
12. Auerswald L, Schneider P, Gäde G. 1998b. Utilisation of substrates during tethered flight with and without lift generation in the African fruit beetle Pachnoda sinuata (Cetoniinae). J Exp Biol 201:2333-2342
13. Auerswald L, Siegert KJ, Gäde G. 2005. Activation of triacylglycerol lipase in the fat body of a beetle by adipokinetic hormone. Insect Biochem Mol Biol 35:461-470
14. Bartholomew GA, Casey TM. 1978. Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J Exp Biol 76:11-25
15. Belmont M, Cazzamali G, Williamson M, Hauser F, Grimmelikhuijzen CJP. 2006. Identification of four evolutionarily related G protein-coupled receptors from the malaria mosquito Anopheles gambiae. Biochem Biophys Res Commun 344:160-165
16. Bharucha KN, Tarr P, Zipursky SL. 2008. A glucagon-like endocrine pathway in Drosophila modulates both lipid and carbohydrate homeostasis. J Exp Biol 211:3103-3110
17. Birkenbeil H. 1971. Untersuchungen zur Wirkung von Neurohormon D und von anderen aktiven Substanzen auf das Zentralnervensystem der Schabe Periplaneta americana (L.). Zool Jb Physiol 58:493-525
18. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, Hafen E. 2001. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11:213-221
19. Bursell E. 1981. The role of proline in energy metabolism. In: Downer RGH, editor. Energy metabolism of insects. New York: Plenum Press. p. 135-154
20. Canavoso LE, Stariolo R, Rubiolo ER. 2003. Flight metabolism in Panstrongylus megistus (Hemiptera: Reduviidae): the role of carbohydrates and lipids. Mem Inst Osvaldo Cruz 98:909-914
21. Candy DJ. 2002. Adipokinetic hormones concentrations in the haemolymph of Schistocerca gregaria, measured by radioimmunoassay. Insect Biochem Mol Biol 32:1361-1367
22. Cannon WB. 1927. Bodily changes in pain, hunger, fear and rage. New-York, London: D. Appleton and Company
23. Carlisle JA, Loughton BG. 1979. Adipokinetic hormone inhibits protein synthesis in Locusta. Nature 282:420-421
24. Fernlund P, Josefsson L. 1972. Crustacean color-change hormone: amino acid sequence and chemical synthesis. Science 177:173-175
25. Foa PP. 1973. Glucagon: an incomplete and biased review with selected references. Amer Zool 13:613-23
26. Gäde G. 1981. Activation of fat body glycogen phosphorylase in Locusta migratoria by corpus cardiacum extract and synthetic adipokinetic hormone. J Insect Physiol 27:155-161
27. Gäde G. 1997a. Distinct sequences of AKH/RPCH family members in beetle (Scarabaeus-species) corpus cardiacum contain three aromatic amino acid residues. Biochem Biophys Res Commun 230:16-21
28. Gäde G. 1997b. Hyperprolinaemia caused by novel members of the adipokinetic hormone/red pigment-concentrating hormone family of peptides isolated from corpora cardiaca of onitine beetles. Biochem J 321:201-206
29. Gäde G. 2004. Flight or fight - the need for adipokinetic hormones. Int Cong Ser 1275:134-140
30. Gäde G. 2007. Flight fuel and neuropeptidergic control of fuel mobilisation in the homopteran spittle bug, Locris arithmetica. Abstracts of the 100th Annual Meeting of the German Zoological Society, Cologne, O44
31. Gäde G. 2009. Peptides of the adipokinetic/red pigmentconcentrating hormone family - a new take on biodiversity. Ann N Y Acad Sci 1163:125-136
32. Gäde G, Auerswald L. 2002. Beetles' choice - proline for energy output: control by AKHs. Comp Biochem Physiol B 132:117-129
33. Gäde G, Auerswald L. 2003. Mode of action of neuropeptides from the adipokinetic hormone family. Gen Comp Endocrinol 132:10-20
34. Gäde G, Auerswald L, Marco HG. 2006b. Flight fuel and neuropeptidergic control of fuel mobilisation in the twig wilter, Holopterna alata (Hemiptera, Coreidae). J Insect Physiol 52:1171-1181
35. Gäde G, Auerswald L, Predel R, Marco HG. 2004. Substrate usage and its regulation during flight and swimming in the backswimmer, Notonecta glauca. Physiol Entomol 29:84-93
36. Gäde G, Auerswald L, Şimek P, Marco HG, Kodrík D. 2003. Red pigment-concentrating hormone is not limited to crustaceans. Biochem Biophys Res Commun 309:967-973
37. Gäde G, Beenakkers AMT. 1977. Adipokinetic hormoneinduced lipid mobilization and cyclic AMP accumulation in the fat body of Locusta migratoria during development. Gen Comp Endocrinol 32:481-487
38. Gäde G, Clark K, Şimek P, Auerswald L. 2006a. Unique translational modification of an invertebrate neuropeptide: a phosphorylated member of the adipokinetic hormone peptide family. Biochem J 393:705-713
39. Gäde G, Hoffmann KH. 2005. Neuropeptides regulating development and reproduction in insects. Physiol Entomol 130:103-121
40. Gäde G, Hoffmann KH, Spring JH. 1997. Hormonal regulation in insects: facts, gaps, and future directions. Physiol Rev 77:963-1032
41. Gäde G, Janssens MPE. 1994. Cicadas contain novel members of the AKH/RPCH family peptides with hypertrehalosaemic activity. Biol Chem Hoppe-Seyler 375:803-809
42. Gäde G, Lopata A, Kellner R, Rinehart KL. 1992. Primary structures of neuropeptides isolated from the corpora cardiaca of various cetonid beetle species determined by pulsed-liquid phase sequencing and tandem fast atom bombardment mass spectrometry. Biol Chem Hoppe-Seyler 373:133-142
43. Gäde G, Şimek P, Marco HG. 2007a. A novel adipokinetic peptide in a water boatman (Heteroptera, Corixidae) and its bioanalogue in a saucer bug (Heteroptera, Naucoridae). Peptides 28:594-601
44. Gäde G, Şimek P, Marco HG. 2007b. Water scorpions (Heteroptera, Nepidae) and giant water bugs (Heteroptera, Belostomatidae): sources of new members of the adipokinetic hormone/red pigment-concentrating hormone family. Peptides 28:1359-1367
45. Gilbert LI, Chino H. 1974. Transport of lipids in insects. J Lipid Res 15:439-456
46. Glinka AV, Kleiman AM, Wyatt GR. 1995. Roles of juvenile hormone, a brain factor and adipokinetic hormone in regulation of vitellogenin biosynthesis in Locusta migratoria. Biochem Mol Biol Int 35:323-328
47. Gokuldas M, Hunt PA, Candy DJ. 1988. The inhibition of lipid synthesis in vitro in the locust, Schistocerca gregaria, by factors from the corpora cardiaca. Physiol Entomol 13:43-48
48. Goldsworthy GJ. 1983. The endocrine control of flight metabolism in locusts. Adv Insect Physiol 17:149-204
49. Goldsworthy G. 1994. Adipokinetic hormones of insects: are they the insect glucagons? In: Davey KG, Tobe SS, Peter AG, editors. Perspectives in comparative endocrinology. Ottawa: National Research Council of Canada. p. 486-492
50. Goldsworthy GJ, Kodrík D, Comley R, Lightfoot M. 2002. A quantitative study of adipokinetic hormone of the firebug, Pyrrhocoris apterus. J Insect Physiol 48:1103-1109
51. Grönke S, Müller G, Hirsch J, Fellert S, Andreou A, Haase T, Jäckle H, Kühnlein RP. 2007. Dual lipolytic control of body fat storage and mobilization in Drosophila. PLoS Biol 5:e137
52. Hansen KK, Hauser F, Cazzamali G, Williamson M, Grimmelikhuijzen CJP. 2006. Cloning and characterization of the adipokinetic hormone receptor from the cockroach Periplaneta americana. Biochem Biophys Res Commun 343:638-643
53. Hill L, Goldsworthy GJ. 1968. Growth, feeding activity, and the utilization of reserves in larvae of Locusta. J Insect Physiol 14:1085-1098
54. Husak JF, Irschick DJ, McCormick SD, Moore IT. 2009. Hormonal regulation of whole-animal performance: implications for selection. Integrative and Comparative Biology doi:10.1093/icb/icp030
55. Isabel G, Martin JR, Chidami S, Veenstra JA, Rosay P. 2005. AKH-producing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am J Physiol Regul Integr Comp Physiol 288:R531-8
56. Johnson CG. 1969. Migration and dispersal of insects by flight. London: Methuen
57. Karl I, Lorenz MW, Fischer K. 2007. Energetics of reproduction: consequences of divergent selection on egg size, food limitation, and female age for egg composition and reproductive effort in a butterfly. Biol J Linn Soc 91:403-418
58. Kaufmann C, Brown MR. 2006. Adipokinetic hormones in the African malaria mosquito, Anopheles gambiae: identification and expression of genes for two peptides and a putative receptor. Insect Biochem Mol Biol 36:466-481
59. Kodrík D. 2008. Adipokinetic hormone functions that are not associated with insect flight. Physiol Entomol 33:171-180
60. Kodrík D, Socha R, Şimek P, Zemek R, Goldsworthy GJ. 2000. A new member of the AKH/RPCH family that stimulates locomotory activity in the firebug, Pyrrhocoris apterus (Heteroptera). Insect Biochem Mol Biol 30:489-498
61. Kodrík D, Socha R, Syrová Z. 2003. Developmental and diel changes of adipokinetic hormone in CNS and haemolymph of the flightless wing-polymorphic bug, Pyrrhocoris apterus (L.). J Insect Physiol 49:53-61
62. Kodrík D, Socha R, Zemek R. 2002. Topical application of Pya-AKH stimulates lipid mobilization and locomotion in the flightless bug, Pyrrhocoris apterus (L.) (Heteroptera). Physiol Entomol 27:15-20
63. Lee G, Park JH. 2004. Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167:311-323
64. Lindemans M, Liu F, Janssen T, Husson ST, Mertens I, Gäde G, Schoofs L. 2009. Adipokinetic hormone signaling through the gonadotropin-releasing hormone receptor modulates egg-laying in Caenorhabditis elegans. Proc Natl Acad Sci USA 106:1642-1647
65. Lohr P, Gäde G. 1983. Carbohydrate metabolism in the stick insect, Carausius morosus. J Insect Physiol 29: 287-293
66. Lopata AL, Gäde G. 1994. Physiological action of a neuropeptide from the corpora cardiaca of the fruit beetle, Pachnoda sinuata, and its possible role in flight metabolism. J Insect Physiol 40:53-62
67. Lorenz MW. 2001. Synthesis of lipids in the fat body of Gryllus bimaculatus: age-dependency and regulation by adipokinetic hormone. Arch Insect Biochem Physiol 47:198-214
68. Lorenz MW. 2003. Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus. Comp Biochem Physiol B 136:197-206
69. Lorenz MW. 2004. Erratum to ''Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus'': [Comp. Biochem. Physiol 136B(2003):197-206]. Comp Biochem Physiol B 137:285-286
70. Lorenz MW. 2007. Oogenesis-flight syndrome in crickets: age-dependent egg production, flight performance, and biochemical composition of the flight muscles in adult female Gryllus bimaculatus. J Insect Physiol 53:819-832
71. Lorenz MW, Anand AN. 2004. Changes in the biochemical composition of fat body stores during adult development of female crickets, Gryllus bimaculatus. Arch Insect Biochem Physiol 56:110-119
72. Lorenz MW, Kellner R, Temnow K, Woodring J. 2009. Identification of the adipokinetic hormone of the large milkweed bug Oncopeltus fasciatus. Physiol Entomol 34:136-143
73. Lorenz MW, Zemek R, Kodrík D, Socha R. 2004. Lipid mobilization and locomotor stimulation in Gryllus bimaculatus by topically applied adipokinetic hormone. Physiol Entomol 29:146-151
74. Maxová A, Kodrík D, Zemek R, Socha R. 2001. Diel changes in adipokinetic response and walking activity of Pyrrhocoris apterus (Heteroptera) in relation to physiological status and wing dimorphism. Eur J Entomol 98:433-438
75. Mayer RJ, Candy DJ. 1969. Control of haemolymph lipid concentration during locust flight: an adipokinetic hormone from the corpora cardiaca. J Insect Physiol 15:611-620
76. Moshitzky P, Applebaum SW. 1990. The role of adipokinetic hormone in the control of vitellogenesis in locusts. Insect Biochem 20:319-323
77. Mwangi RW, Goldsworthy GJ. 1977. Age-related changes in the response to adipokinetic hormone in Locusta migratoria. Physiol Entomol 2:37-42
78. Nestel D, Tolmasky D, Rabossi A, Quesada-Allué LA. 2003. Lipid, carbohydrates and protein patterns during metamorphosis of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Ann Entomol Soc Am 96:237-244 (Pubitemid 36938375)
79. Orchard I, Ramirez JM, Lange AB. 1993. A multifunctional role for octopamine in locust flight. Annu Rev Entomol 38:227-249
80. Roeder T. 2005. Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447-477
81. Roff DA. 1986. The evolution of wing dimorphism in insects. Evolution 40:1009-1020
82. Rulifson EJ, Kim SK, Nusse R. 2002. Ablation of insulinproducing neurons in flies: growth and diabetic phenotypes. Science 296:1118-1120
83. Saraswati S, Fox LE, Soll DR, Wu C-F. 2004. Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58:425-441
84. Sloggett JJ, Lorenz MW. 2008. Egg composition and reproductive investment in aphidophagous ladybird beetles (Coccinellidae: Coccinellini): egg development and interspecific variation. Physiol Entomol 33:200-208
85. Socha R, Kodrík D, Zemek R. 1999. Adipokinetic hormone stimulates insect locomotor activity. Naturwissenschaften 88:85-86
86. Staubli F, Jorgensen TJD, Cazzamali G, Williamson M, Lenz C, Sondergaard L, Roepstorff P, Grimmelikhuijzen CJP. 2002. Molecular identification of the insect adipokinetic hormone receptors. Proc Natl Acad Sci USA 99:3446-3451 (Pubitemid 34252128)
87. Stay B, Tobe SS. 2007. The role of allatostatins in juvenile hormone synthesis in insects and crustaceans. Annu Rev Entomol 52:277-299
88. Steele JE. 1961. Occurence of a hyperglycaemic factor in the corpus cardiacum of an insect. Nature 18:680-681
89. Van der Horst DJ. 2003. Insect adipokinetic hormones: release and integration of flight energy metabolism. Comp Biochem Physiol B 136:217-226
90. Van Marrewijk WJA, Van den Broek ATM, Van der Horst DJ, Beenakkers AMT. 1984. Hypertrehalosaemic and hyperlipaemic responses to adipokinetic hormone in fifth larval instar locusts, Locusta migratoria. Insect Biochem 14:151-157
91. Walker PR, Hill L, Bailey E. 1970. Feeding activity, respiration, and lipid and carbohydrate content of the male desert locust during adult development. J Insect Physiol 16:1001-1015
92. Ward JP, Candy DJ, Smith SN. 1982. Lipid storage and changes during flight by triatomine bugs (Rhodnius prolixus and Triatoma infestans). J Insect Physiol 28:527-534
93. Wicher D, Agricola HJ, Schönherr R, Heinemann SH, Derst C. 2006b. TRP- channels are inhibited by cAMP and contribute to pacemaking in neurosecretory insect neurons. J Biol Chem 281:3227-3236
94. Wicher D, Agricola H-J, Söhler S, Gundel M, Heinemann SH, Wollweber L, Stengl M, Derst C. 2006a. Differential receptor activation by cockroach adipokinetic hormones produces differential effects on ion currents, neuronal activity, and locomotion. J Neurophysiol 95:2314-2325
95. Wicher D, Berlau J, Walther C, Borst A. 2006c. Peptidergic counter-regulation of Ca2+- and Na+-dependent K+ currents modulates the shape of action potentials in neurosecretory insect neurons. J Neurophysiol 95:311-322
96. Wicher D, Walther C, Penzlin H. 1994. Neurohormone D induces ionic current changes in cockroach central neurones. J Comp Physiol A 174:507-515
97. Woodring J, Hoffmann KH, Lorenz MW. 2007. Activity, release and flow of digestive enzymes in the cricket, Gryllus bimaculatus. Physiol Entomol 32:56-63 (Pubitemid 46463830)
98. Woodring J, Lorenz MW. 2007. Feeding, nutrient flow, and functional gut morphology in the cricket Gryllus bimaculatus. J Morphol 268:815-825
99. Woodring J, Lorenz MW, Hoffmann KH. 2002. Sensitivity of larval and adult crickets (Gryllus bimaculatus) to adipokinetic hormone. Comp Biochem Physiol A 133: 637-644
100. Wu Q, Brown MR. 2006. Signaling and function of insulinlike peptides in insects. Annu Rev Entomol 51:1-24
101. Zebe E, Gäde G. 1993. Flight metabolism in the African fruit beetle, Pachnoda sinuata. J Comp Physiol B 163: 107-112
102. Zera AJ. 2004. The endocrine regulation of wing polymorphism in insects: state of the art, recent surprises, and future directions. Integr Comp Biol 43:607-616
103. Zera AJ, Denno RF. 1997. Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207-231
104. Ziegler R. 1997. Lipid synthesis by ovaries and fat body of Aedes aegypti (Diptera: Culicidae). Eur J Entomol 94:385-391
105. Ziegler R, Eckhart K, Law JH. 1990. Adipokinetic hormone controls lipid metabolism in adults and carbohydrate metabolism in larvae of Manduca sexta. Peptides 11:1037-1040