1932

Abstract

Insects, like all eukaryotes, require sterols for structural and metabolic purposes. However, insects, like all arthropods, cannot make sterols. Cholesterol is the dominant tissue sterol for most insects; insect herbivores produce cholesterol by metabolizing phytosterols, but not always with high efficiency. Many insects grow on a mixed-sterol diet, but this ability varies depending on the types and ratio of dietary sterols. Dietary sterol uptake, transport, and metabolism are regulated by several proteins and processes that are relatively conserved across eukaryotes. Sterol requirements also impact insect ecology and behavior. There is potential to exploit insect sterol requirements to () control insect pests in agricultural systems and () better understand sterol biology, including in humans. We suggest that future studies focus on the genetic mechanism of sterol metabolism and reverse transportation, characterizing sterol distribution and function at the cellular level, the role of bacterial symbionts in sterol metabolism, and interrupting sterol trafficking for pest control.

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2020-01-07
2024-10-14
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Literature Cited

  1. 1. 
    Adams AS, Jordan MS, Adams SM, Suen G, Goodwin L et al. 2011. Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio. ISME J 5:1323–31
    [Google Scholar]
  2. 2. 
    Alberts B, Johnson AD, Lewis J, Morgan D, Raff M et al. 2015. Molecular Biology of the Cell New York: Garland Sci.
    [Google Scholar]
  3. 3. 
    Behmer ST. 2017. Overturning dogma: Tolerance of insects to mixed-sterol diets is not universal. Curr. Opin. Insect Sci. 23:89–95A mini-review based on three different experiments that infers how dietary sterol structure impacts insect performance, with implications for cell membranes.
    [Google Scholar]
  4. 4. 
    Behmer ST, Elias DO. 1999. The nutritional significance of sterol metabolic constraints in the generalist grasshopper Schistocerca americana. J. Insect Physiol 45:339–48
    [Google Scholar]
  5. 5. 
    Behmer ST, Elias DO. 1999. Phytosterol structure and its impact on feeding behaviour in the generalist grasshopper Schistocerca americana. Physiol. Entomol 24:18–27
    [Google Scholar]
  6. 6. 
    Behmer ST, Elias DO. 2000. Sterol metabolic constraints as a factor contributing to the maintenance of diet mixing in grasshoppers (Orthoptera: Acrididae). Physiol. Biochem. Zool. 73:219–30
    [Google Scholar]
  7. 7. 
    Behmer ST, Elias DO, Bernays EA 1999. Post-ingestive feedbacks and associative learning regulate the intake of unsuitable sterols in a generalist grasshopper. J. Exp. Biol. 202:739–48
    [Google Scholar]
  8. 8. 
    Behmer ST, Elias DO, Grebenok RJ 1999. Phytosterol metabolism and absorption in the generalist grasshopper, Schistocerca americana (Orthoptera: Acrididae). Arch. Insect Biochem. Physiol. 42:13–25
    [Google Scholar]
  9. 9. 
    Behmer ST, Grebenok RJ. 1998. Impact of dietary sterols on life-history traits of a caterpillar. Physiol. Entomol. 23:165–75
    [Google Scholar]
  10. 10. 
    Behmer ST, Grebenok RJ, Douglas AE 2011. Plant sterols and host plant suitability for a phloem-feeding insect. Funct. Ecol. 25:484–91
    [Google Scholar]
  11. 11. 
    Behmer ST, Nes WD. 2003. Insect sterol nutrition and physiology: a global overview. Advances in Insect Physiology S Simpson 1–72 Amsterdam: ElsevierThe last comprehensive review on insect sterol physiology.
    [Google Scholar]
  12. 12. 
    Bennett WFD, MacCallum JL, Hinner MJ, Marrink SJ, Tieleman DP 2009. Molecular view of cholesterol flip-flop and chemical potential in different membrane environments. J. Am. Chem. Soc. 131:12714–20
    [Google Scholar]
  13. 13. 
    Bentz BJ, Six DL. 2006. Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae). Ann. Entomol. Soc. Am. 99:189–94
    [Google Scholar]
  14. 14. 
    Benveniste P. 2004. Biosynthesis and accumulation of sterols. Annu. Rev. Plant Biol. 55:429–57
    [Google Scholar]
  15. 15. 
    Berge KE, Tian H, Graf GA, Yu L, Grishin NV et al. 2000. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC Transporters. Science 290:1771–75
    [Google Scholar]
  16. 16. 
    Blitzer EJ, Vyazunova I, Lan Q 2005. Functional analysis of AeSCP-2 using gene expression knockdown in the yellow fever mosquito, Aedes aegypti. Insect Mol. Biol. 14:301–7
    [Google Scholar]
  17. 17. 
    Bonneton F, Laudet V. 2012. Evolution of nuclear receptors in insects. Insect Endocrinology LI Gilbert 219–52 Amsterdam: Elsevier
    [Google Scholar]
  18. 18. 
    Bouvaine S, Behmer ST, Lin GG, Faure M-L, Grebenok RJ, Douglas AE 2012. The physiology of sterol nutrition in the pea aphid Acyrthosiphon pisum. J. Insect Physiol 58:1383–89
    [Google Scholar]
  19. 19. 
    Bouvaine S, Faure M-L, Grebenok RJ, Behmer ST, Douglas AE 2014. A dietary test of putative deleterious sterols for the aphid Myzus persicae. PLOS ONE 9:e86256
    [Google Scholar]
  20. 20. 
    Bujold M, Gopalakrishnan A, Nally E, King-Jones K 2010. Nuclear receptor DHR96 acts as a sentinel for low cholesterol concentrations in Drosophila melanogaster. Mol. Cell. Biol 30:793–805
    [Google Scholar]
  21. 21. 
    Campbell BC, Nes WD. 1983. A reappraisal of sterol biosynthesis and metabolism in aphids. J. Insect Physiol. 29:149–56
    [Google Scholar]
  22. 22. 
    Canavoso LE, Bertello LE, de Lederkremer RM, Rubiolo ER 1998. Effect of fasting on the composition of the fat body lipid of Dipetalogaster maximus, Triatoma infestans and Panstrongylus megistus (Hemiptera: Reduviidae). J. Comp. Physiol. B 168:549–54
    [Google Scholar]
  23. 23. 
    Caragata EP, Rancès E, Hedges LM, Gofton AW, Johnson KN et al. 2013. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLOS Pathog 9:e1003459
    [Google Scholar]
  24. 24. 
    Carvalho M, Sampaio JL, Palm W, Brankatschk M, Eaton S, Shevchenko A 2012. Effects of diet and development on the Drosophila lipidome. Mol. Syst. Biol. 8:600
    [Google Scholar]
  25. 25. 
    Carvalho M, Schwudke D, Sampaio JL, Palm W, Riezman I et al. 2010. Survival strategies of a sterol auxotroph. Development 137:3675–85
    [Google Scholar]
  26. 26. 
    Chen L-L, Wang G-Z, Zhang H-Y 2007. Sterol biosynthesis and prokaryotes-to-eukaryotes evolution. Biochem. Biophys. Res. Commun. 363:885–88
    [Google Scholar]
  27. 27. 
    Ciufo L, Murray P, Thompson A, Rigden D, Rees H 2011. Characterisation of a desmosterol reductase involved in phytosterol dealkylation in the silkworm, Bombyx mori. PLOS ONE 6:e21316
    [Google Scholar]
  28. 28. 
    Clifton ME, Noriega FG. 2012. The fate of follicles after a blood meal is dependent on previtellogenic nutrition and juvenile hormone in Aedes aegypti. J. Insect Physiol 58:1007–19
    [Google Scholar]
  29. 29. 
    Cooper MK, Wassif CA, Krakowiak PA, Taipale J, Gong R et al. 2003. A defective response to Hedgehog signaling in disorders of cholesterol biosynthesis. Nat. Genet. 33:508–13
    [Google Scholar]
  30. 30. 
    Crowder CM, Westover EJ, Kumar AS, Ostlund RE, Covey DF 2001. Enantiospecificity of cholesterol function in vivo. J. Biol. Chem. 276:44369–72
    [Google Scholar]
  31. 31. 
    Deffieu MS, Pfeffer SR. 2011. Niemann-Pick type C 1 function requires lumenal domain residues that mediate cholesterol-dependent NPC2 binding. PNAS 108:18932–36
    [Google Scholar]
  32. 32. 
    Desmond E, Gribaldo S. 2009. Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature. Genome Biol. Evol. 1:364–81
    [Google Scholar]
  33. 33. 
    Dobrosotskaya IY, Seegmiller AC, Brown MS, Goldstein JL, Rawson RB 2002. Regulation of SREBP processing and membrane lipid production by phospholipids in Drosophila. Science 296:879–83Insect SREBP regulates phosopholipids, not sterols (as in mammals).
    [Google Scholar]
  34. 34. 
    Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34
    [Google Scholar]
  35. 35. 
    Douglas AE. 2018. Omics and the metabolic function of insect–microbial symbioses. Curr. Opin. Insect Sci. 29:1–6
    [Google Scholar]
  36. 36. 
    Du X, Ma H, Zhang X, Liu K, Peng J et al. 2012. Characterization of the sterol carrier protein-x/sterol carrier protein-2 gene in the cotton bollworm, Helicoverpa armigera. J. Insect Physiol. 58:1413–23
    [Google Scholar]
  37. 37. 
    Dupont S, Lemetais G, Ferreira T, Cayot P, Gervais P, Beney L 2012. Ergosterol biosynthesis: a fungal pathway for life on land?. Evolution 66:2961–68
    [Google Scholar]
  38. 38. 
    Duval C, Touche V, Tailleux A, Fruchart J-C, Fievet C et al. 2006. Niemann–Pick C1 like 1 gene expression is down-regulated by LXR activators in the intestine. Biochem. Biophys. Res. Commun. 340:1259–63
    [Google Scholar]
  39. 39. 
    Dyer DH, Lovell S, Thoden JB, Holden HM, Rayment I, Lan Q 2003. The structural determination of an insect sterol carrier protein-2 with a ligand-bound C16 fatty acid at 1.35-angstrom resolution. J. Biol. Chem. 278:39085–91
    [Google Scholar]
  40. 40. 
    Dyer DH, Vyazunova I, Lorch JM, Forest KT, Lan Q 2009. Characterization of the yellow fever mosquito sterol carrier protein-2 like 3 gene and ligand-bound protein structure. Mol. Cell. Biochem. 326:67–77
    [Google Scholar]
  41. 41. 
    Fahrbach SE, Smagghe G, Velarde RA 2012. Insect nuclear receptors. Annu. Rev. Entomol. 57:83–106
    [Google Scholar]
  42. 42. 
    Ferreiracaliman MJ, Silva CID, Mateus S, Zucchi R, Nascimento FS 2012. Neutral sterols of cephalic glands of stingless bees and their correlation with sterols from pollen. Psyche 2012:982802
    [Google Scholar]
  43. 43. 
    Ferrer A, Altabella T, Arró M, Boronat A 2017. Emerging roles for conjugated sterols in plants. Prog. Lipid Res. 67:27–37
    [Google Scholar]
  44. 44. 
    Fisk GJ, Thummel CS. 1995. Isolation, regulation, and DNA-binding properties of three Drosophila nuclear hormone receptor superfamily members. PNAS 92:10604–8
    [Google Scholar]
  45. 45. 
    Fluegel ML, Parker TJ, Pallanck LJ 2006. Mutations of a Drosophila NPC1 gene confer sterol and ecdysone metabolic defects. Genetics 172:185–96
    [Google Scholar]
  46. 46. 
    Friedland N, Liou H-L, Lobel P, Stock AM 2003. Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease. PNAS 100:2512–17
    [Google Scholar]
  47. 47. 
    Galea AM, Brown AJ. 2009. Special relationship between sterols and oxygen: Were sterols an adaptation to aerobic life?. Free Radic. Biol. Med. 47:880–89
    [Google Scholar]
  48. 48. 
    Gilbert LI, Warren JT. 2005. A molecular genetic approach to the biosynthesis of the insect steroid molting hormone. Insect Hormones G Litwack 31–57 Amsterdam: Elsevier
    [Google Scholar]
  49. 49. 
    Giraudo M, Audant P, Feyereisen R, Le Goff G 2013. Nuclear receptors HR96 and ultraspiracle from the fall armyworm (Spodoptera frugiperda), developmental expression and induction by xenobiotics. J. Insect Physiol. 59:560–68
    [Google Scholar]
  50. 50. 
    Gong J, Hou Y, Zha XF, Lu C, Zhu Y, Xia QY 2006. Molecular cloning and characterization of Bombyx mori sterol carrier protein x/sterol carrier protein 2 (SCPx/SCP2) gene. DNA Seq 17:326–33
    [Google Scholar]
  51. 51. 
    Gong X, Qian H, Zhou X, Wu J, Wan T et al. 2016. Structural insights into the Niemann-Pick C1 (NPC1)-mediated cholesterol transfer and ebola infection. Cell 165:1467–78
    [Google Scholar]
  52. 52. 
    Gottschling D, Doring F. 2019. Is C. elegans a suitable model for nutritional science?. Genes Nutr 14:1
    [Google Scholar]
  53. 53. 
    Gregor A, Kramer JM, Voet M, Schanze I, Uebe S et al. 2014. Altered GPM6A/M6 dosage impairs cognition and causes phenotypes responsive to cholesterol in human and Drosophila. . Hum. Mutat 35:1495–505
    [Google Scholar]
  54. 54. 
    Guan XL, Cestra G, Shui G, Kuhrs A, Schittenhelm RB et al. 2013. Biochemical membrane lipidomics during Drosophila development. Dev. Cell 24:98–111
    [Google Scholar]
  55. 55. 
    Guo X-R, Zheng S-C, Liu L, Feng Q-L 2009. The sterol carrier protein 2/3-oxoacyl-CoA thiolase (SCPx) is involved in cholesterol uptake in the midgut of Spodoptera litura: gene cloning, expression, localization and functional analyses. BMC Mol. Biol. 10:102
    [Google Scholar]
  56. 56. 
    Harrison JF, Kaiser A, VandenBrooks JM 2010. Atmospheric oxygen level and the evolution of insect body size. Proc. Biol. Sci. 277:1937–46
    [Google Scholar]
  57. 57. 
    Herren JK, Paredes JC, Schüpfer F, Arafah K, Bulet P, Lemaitre B 2014. Insect endosymbiont proliferation is limited by lipid availability. eLife 3:e02964
    [Google Scholar]
  58. 58. 
    Heyer J, Parker B, Becker D, Ruffino J, Fordyce A et al. 2004. Steroid profiles of transgenic tobacco expressing an Actinomyces 3-hydroxysteroid oxidase gene. Phytochemistry 65:2967–76
    [Google Scholar]
  59. 59. 
    Hobson RP. 1935. On a fat-soluble growth factor required by blow-fly larvae. I. Distribution and properties. Biochem. J. 29:1292–96
    [Google Scholar]
  60. 60. 
    Hofsäß C, Lindahl E, Edholm O 2003. Molecular dynamics simulations of phospholipid bilayers with cholesterol. Biophys. J. 84:2192–206
    [Google Scholar]
  61. 61. 
    Horner MA, Pardee K, Liu S, King-Jones K, Lajoie G et al. 2009. The Drosophila DHR96 nuclear receptor binds cholesterol and regulates cholesterol homeostasis. Genes Dev 23:2711–16Describes DHR96 as a detector of low cholesterol levels and a regulator of cholesterol homeostasis.
    [Google Scholar]
  62. 62. 
    Hortsch R, Lee E, Erathodiyil N, Hebbar S, Steinert S et al. 2010. Glycolipid trafficking in Drosophila undergoes pathway switching in response to aberrant cholesterol levels. Mol. Biol. Cell 21:778–90
    [Google Scholar]
  63. 63. 
    Huang X, Suyama K, Buchanan J, Zhu AJ, Scott MP 2005. A Drosophila model of the Niemann-Pick type C lysosome storage disease: dnpc1a is required for molting and sterol homeostasis. Development 132:5115–24
    [Google Scholar]
  64. 64. 
    Huang X, Warren JT, Buchanan J, Gilbert LI, Scott MP 2007. Drosophila Niemann-Pick Type C-2 genes control sterol homeostasis and steroid biosynthesis: a model of human neurodegenerative disease. Development 134:3733–42The first insect study to experimentally verify the function of NPC2 genes in sterol homeostasis.
    [Google Scholar]
  65. 65. 
    Ikonen E. 2008. Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9:125–38
    [Google Scholar]
  66. 66. 
    Ioannou YA. 2007. Niemann-Pick C proteins in sterol transport and absorption: flies in the ointment. Dev. Cell 12:481–83
    [Google Scholar]
  67. 67. 
    Janson E, Grebenok R, Behmer S, Abbot P 2009. Same host-plant, different sterols: variation in sterol metabolism in an insect herbivore community. J. Chem. Ecol. 35:1309–19
    [Google Scholar]
  68. 68. 
    Jing X, Grebenok RJ, Behmer ST 2012. Plant sterols and host plant suitability for generalist and specialist caterpillars. J. Insect Physiol. 58:235–44
    [Google Scholar]
  69. 69. 
    Jing X, Grebenok RJ, Behmer ST 2013. Sterol/steroid metabolism and absorption in a generalist and specialist caterpillar: effects of dietary sterol/steroid structure, mixture and ratio. Insect Biochem. Mol. Biol. 43:580–87
    [Google Scholar]
  70. 70. 
    Jing X, Grebenok RJ, Behmer ST 2014. Diet micronutrient balance matters: how the ratio of dietary sterols/steroids affects development, growth and reproduction in two lepidopteran insects. J. Insect Physiol. 67:85–96
    [Google Scholar]
  71. 71. 
    Jing X, Vogel H, Grebenok RJ, Zhu-Salzman K, Behmer ST 2012. Dietary sterols/steroids and the generalist caterpillar Helicoverpa zea: physiology, biochemistry and midgut gene expression. Insect Biochem. Mol. Biol. 42:835–45The first genome-wide study on sterol metabolism in an insect.
    [Google Scholar]
  72. 72. 
    Jouni ZE, Yun HK, Wells MA 2002. Cholesterol efflux from larval Manduca sexta fat body in vitro: high-density lipophorin as the acceptor. J. Insect Physiol. 48:609–18
    [Google Scholar]
  73. 73. 
    Jouni ZE, Zamora J, Wells MA 2002. Absorption and tissue distribution of cholesterol in Manduca sexta. Arch. Insect Biochem. Physiol 49:167–75
    [Google Scholar]
  74. 74. 
    Jupatanakul N, Sim S, Dimopoulos G 2014. Aedes aegypti ML and Niemann-Pick type C family members are agonists of dengue virus infection. Dev. Comp. Immunol. 43:1–9
    [Google Scholar]
  75. 75. 
    Kalaany NY, Mangelsdorf DJ. 2006. LXRS and FXR: the Yin and Yang of cholesterol and fat metabolism. Annu. Rev. Physiol. 68:159–91
    [Google Scholar]
  76. 76. 
    Kim M-S, Lan Q. 2010. Sterol carrier protein-x gene and effects of sterol carrier protein-2 inhibitors on lipid uptake in Manduca sexta. BMC Physiol 10:9
    [Google Scholar]
  77. 77. 
    Kim M-S, Lan Q. 2011. Larvicidal activity of α-mangostin in the Colorado potato beetle, Leptinotarsa decemlineata. J. Pestic. Sci. 36:1231–39
    [Google Scholar]
  78. 78. 
    Kim M-S, Wessely V, Lan Q 2005. Identification of mosquito sterol carrier protein-2 inhibitors. J. Lipid Res. 46:650–57
    [Google Scholar]
  79. 79. 
    King-Jones K, Horner MA, Lam G, Thummel CS 2006. The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. Cell Metab 4:37–48
    [Google Scholar]
  80. 80. 
    Ko DC, Binkley J, Sidow A, Scott MP 2003. The integrity of a cholesterol-binding pocket in Niemann-Pick C2 protein is necessary to control lysosome cholesterol levels. PNAS 100:2518–25
    [Google Scholar]
  81. 81. 
    Korber M, Klein I, Daum G 2017. Steryl ester synthesis, storage and hydrolysis: a contribution to sterol homeostasis. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1862:1534–45
    [Google Scholar]
  82. 82. 
    Lafont R, Dauphin-Villemant C, Warren JT, Rees H 2005. Ecdysteroid chemistry and biochemistry. Comprehensive Molecular Insect Science LI Gilbert, K Latrou, SS Gill 125–95 Amsterdam: Elsevier
    [Google Scholar]
  83. 83. 
    Lan Q, Massey RJ. 2004. Subcellular localization of the mosquito sterol carrier protein-2 and sterol carrier protein-x. J. Lipid Res. 45:1468–74
    [Google Scholar]
  84. 84. 
    Lan Q, Wessely V. 2004. Expression of a sterol carrier protein-x gene in the yellow fever mosquito, Aedes aegypti. Insect Mol. Biol. 13:519–29
    [Google Scholar]
  85. 85. 
    Lang M, Murat S, Clark AG, Gouppil G, Blais C et al. 2012. Mutations in the neverland gene turned Drosophila pachea into an obligate specialist species. Science 337:1658–61Illustrates how sterol nutrition can be a selective force driving a generalist feeder to become a specialist.
    [Google Scholar]
  86. 86. 
    Larson RT, Lorch JM, Pridgeon JW, Becnel JJ, Clark GG, Lan Q 2010. The biological activity of alpha-Mangostin, a larvicidal botanic mosquito sterol carrier protein-2 inhibitor. J. Med. Entomol. 47:249–57
    [Google Scholar]
  87. 87. 
    Lee MJ, Park SH, Han JH, Hong YK, Hwang S et al. 2011. The effects of hempseed meal intake and linoleic acid on Drosophila models of neurodegenerative diseases and hypercholesterolemia. Mol. Cells 31:337–42
    [Google Scholar]
  88. 88. 
    Lee MJ, Park MS, Hwang S, Hong YK, Choi G et al. 2010. Dietary hempseed meal intake increases body growth and shortens the larval stage via the upregulation of cell growth and sterol levels in Drosophila melanogaster. Mol. Cells 30:29–36
    [Google Scholar]
  89. 89. 
    Liu S, Li K, Gao Y, Liu X, Chen W et al. 2018. Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in Drosophila. PNAS 115:139–44
    [Google Scholar]
  90. 90. 
    Ma H, Ma Y, Liu X, Dyer DH, Xu P et al. 2015. NMR structure and function of Helicoverpa armigera sterol carrier protein-2, an important insecticidal target from the cotton bollworm. Sci. Rep. 5:18186
    [Google Scholar]
  91. 91. 
    Ma Z, Liu Z, Huang X 2010. OSBP- and FAN-mediated sterol requirement for spermatogenesis in Drosophila. Development 137:3775–84
    [Google Scholar]
  92. 92. 
    Matthaus B, Bruhl L. 2008. Virgin hemp seed oil: an interesting niche product. Eur. J. Lipid Sci. Technol. 110:655–61
    [Google Scholar]
  93. 93. 
    Maurer P, Girault J-P, Larchevêque M, Lafont R 1993. 24-epi-makisterone a (not makisterone A) is the major ecdysteroid in the leaf-cutting ant Acromyrmex octospinosus (reich) (hymenoptera, formicidae: Attini). Arch. Insect Biochem. Physiol. 23:29–35
    [Google Scholar]
  94. 94. 
    Mondy N, Corio-Costet MF. 2000. The response of the grape berry moth (Lobesia botrana) to a dietary phytopathogenic fungus (Botrytis cinerea): the significance of fungus sterols. J. Insect Physiol. 46:1557–64
    [Google Scholar]
  95. 95. 
    Mondy N, Corio-Costet MF, Bodin A, Mandon N, Vannier F, Monge JP 2006. Importance of sterols acquired through host feeding in synovigenic parasitoid oogenesis. J. Insect Physiol. 52:897–904
    [Google Scholar]
  96. 96. 
    Morales-Ramos JA, Rojas MG, Sittertz-Bhatkar H, Saldaña G 2000. Symbiotic relationship between Hypothenemus hampei (Coleoptera: Scolytidae) and Fusarium solani (Moniliales: Tuberculariaceae). Ann. Entomol. Soc. Am. 93:98–100
    [Google Scholar]
  97. 97. 
    Moreau RA, Whitaker BD, Hicks KB 2002. Phytosterols, phytostanols, and their conjugates in foods: structural diversity, quantitative analysis, and health-promoting uses. Prog. Lipid Res. 41:457–500
    [Google Scholar]
  98. 98. 
    Mouritsen OG, Zuckermann MJ. 2004. What's so special about cholesterol?. Lipids 39:1101–13
    [Google Scholar]
  99. 99. 
    Mukherjee S, Maxfield FR. 2004. Lipid and cholesterol trafficking in NPC. Biochim. Biophys. Acta 1685:28–37
    [Google Scholar]
  100. 100. 
    Mullaney BC, Ashrafi K. 2009. C. elegans fat storage and metabolic regulation. Biochim. Biophys. Acta 1791:474–78
    [Google Scholar]
  101. 101. 
    Nasir H, Noda H. 2003. Yeast-like symbiotes as a sterol source in anobiid beetles (Coleoptera, Anobiidae): possible metabolic pathways from fungal sterols to 7-dehydrocholesterol. Arch. Insect Biochem. Physiol. 52:175–82
    [Google Scholar]
  102. 102. 
    Nes WD. 2011. Biosynthesis of cholesterol and other sterols. Chem. Rev. 111:6423–51
    [Google Scholar]
  103. 103. 
    Nguyen AD, McDonald JG, Bruick RK, DeBose-Boyd RA 2007. Hypoxia stimulates degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase through accumulation of lanosterol and hypoxia-inducible factor-mediated induction of insigs. J. Biol. Chem. 282:27436–46
    [Google Scholar]
  104. 104. 
    Nobutaka O, Dennis CK, Matthew T, Matthew PS, Catherine CYC, Ta-Yuan C 2004. Binding between the Niemann-Pick C1 protein and a photoactivatable cholesterol analog requires a functional sterol-sensing domain. PNAS 101:12473–78
    [Google Scholar]
  105. 105. 
    Noda H, Koizumi Y. 2003. Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeastlike symbiotes of rice planthoppers and anobiid beetles. Insect Biochem. Mol. Biol. 33:649–58
    [Google Scholar]
  106. 106. 
    Noguchi T, Miller KG. 2003. A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130:1805–16
    [Google Scholar]
  107. 107. 
    Palm W, Sampaio JL, Brankatschk M, Carvalho M, Mahmoud A et al. 2012. Lipoproteins in Drosophila melanogaster: assembly, function, and influence on tissue lipid composition. PLOS Genet 8:e1002828
    [Google Scholar]
  108. 108. 
    Paredes JC, Herren JK, Schüpfer F, Lemaitre B 2016. The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. mBio 7:e01006–16
    [Google Scholar]
  109. 109. 
    Peng R, Maklokova VI, Chandrashekhar JH, Lan Q 2011. In vivo functional genomic studies of sterol carrier protein-2 gene in the yellow fever mosquito. PLOS ONE 6:e18030
    [Google Scholar]
  110. 110. 
    Phillips SE, Woodruff EA 3rd, Liang P, Patten M, Broadie K 2008. Neuronal loss of Drosophila NPC1a causes cholesterol aggregation and age-progressive neurodegeneration. J. Neurosci. 28:6569–82
    [Google Scholar]
  111. 111. 
    Piironen V, Lindsay DG, Miettinen TA, Toivo J, Lampi A-M 2000. Plant sterols: biosynthesis, biological function and their importance to human nutrition. J. Sci. Food Agric. 80:939–66
    [Google Scholar]
  112. 112. 
    Pilorget L, Buckner J, Lundgren JG 2010. Sterol limitation in a pollen-fed omnivorous lady beetle (Coleoptera: Coccinellidae). J. Insect Physiol. 56:81–87
    [Google Scholar]
  113. 113. 
    Piper MD, Blanc E, Leitao-Goncalves R, Yang M, He X et al. 2014. A holidic medium for Drosophila melanogaster. Nat. Methods 11:100–5
    [Google Scholar]
  114. 114. 
    Price PW, Denno RF, Eubanks MD, Finke DL, Ian K 2011. Insect Ecology: Behavior, Populations and Communities Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  115. 115. 
    Rewitz KF, Rybczynski R, Warren JT, Gilbert LI 2006. The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone. Biochem. Soc. Trans. 34:1256–60
    [Google Scholar]
  116. 116. 
    Rodenburg KW, Van der Horst DJ 2005. Lipoprotein-mediated lipid transport in insects: analogy to the mammalian lipid carrier system and novel concepts for the functioning of LDL receptor family members. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1736:10–29
    [Google Scholar]
  117. 117. 
    Rodríguez-Acebes S, de la Cueva P, Fernández-Hernando C, Ferruelo AJ, Lasunción MA et al. 2009. Desmosterol can replace cholesterol in sustaining cell proliferation and regulating the SREBP pathway in a sterol-Delta24-reductase-deficient cell line. Biochem. J. 420:305–15
    [Google Scholar]
  118. 118. 
    Rosenfeld E, Beauvoit B. 2003. Role of the non-respiratory pathways in the utilization of molecular oxygen by Saccharomyces cerevisiae. Yeast 20:1115–44
    [Google Scholar]
  119. 119. 
    Roth GE, Gierl MS, Vollborn L, Meise M, Lintermann R, Korge G 2004. The Drosophila gene Start1: a putative cholesterol transporter and key regulator of ecdysteroid synthesis. PNAS 101:1601–6
    [Google Scholar]
  120. 120. 
    Seegmiller AC, Dobrosotskaya I, Goldstein JL, Ho YK, Brown MS, Rawson RB 2002. The SREBP pathway in Drosophila: regulation by palmitate, not sterols. Dev. Cell 2:229–38
    [Google Scholar]
  121. 121. 
    Sieber MH, Thummel CS. 2009. The DHR96 nuclear receptor controls triacylglycerol homeostasis in Drosophila. Cell Metab 10:481–90
    [Google Scholar]
  122. 122. 
    Sieber MH, Thummel CS. 2012. Coordination of triacylglycerol and cholesterol homeostasis by DHR96 and the Drosophila LipA homolog magro. Cell Metab 15:122–27
    [Google Scholar]
  123. 123. 
    Smolenaars MMW, Madsen O, Rodenburg KW, Der Horst DJV 2007. Molecular diversity and evolution of the large lipid transfer protein superfamily. J. Lipid Res. 48:489–502
    [Google Scholar]
  124. 124. 
    Svoboda JA. 1994. Steroid metabolism as a target for insect control. Biochem. Soc. Trans. 22:634–41
    [Google Scholar]
  125. 125. 
    Svoboda JA. 1999. Variability of metabolism and function of sterols in insects. Crit. Rev. Biochem. Mol. Biol. 34:49–57
    [Google Scholar]
  126. 126. 
    Svoboda JA, Chitwood DJ. 1992. Inhibition of sterol metabolism in insects and nematodes. Regulation of Isopentenoid Metabolism DW Nes, EJ Parish, JM Trzaskos 205–18 Washington, DC: Am. Chem. Soc.
    [Google Scholar]
  127. 127. 
    Svoboda JA, Lusby WR, Aldrich JR 1983. Neutral sterols of representatives of two groups of hemiptera and their correlation to ecdysteroid content. Arch. Insect Biochem. Physiol. 1:139–45
    [Google Scholar]
  128. 128. 
    Sym M, Basson M, Johnson C 2000. A model for Niemann–Pick type C disease in the nematode Caenorhabditis elegans. Curr. Biol 10:527–30
    [Google Scholar]
  129. 129. 
    Takeuchi H, Chen J-H, Jenkins JR, Bun-Ya M, Turner PC, Rees HH 2004. Characterization of a sterol carrier protein 2/3-oxoacyl-CoA thiolase from the cotton leafworm (Spodoptera littoralis): a lepidopteran mechanism closer to that in mammals than that in dipterans. Biochem. J. 382:93–100
    [Google Scholar]
  130. 130. 
    Talyuli OAC, Bottino-Rojas V, Taracena ML, Soares ALM, Oliveira JHM, Oliveira PL 2015. The use of a chemically defined artificial diet as a tool to study Aedes aegypti physiology. J. Insect Physiol. 83:1–7
    [Google Scholar]
  131. 131. 
    Terra WR, Ferreira C, Jordao BP, Dillon RJ 1996. Digestive enzymes. Biology of the Insect Midgut MJ Lehane, PF Billingsley 153–94 Berlin: Springer
    [Google Scholar]
  132. 132. 
    Thompson BM, Grebenok RJ, Behmer ST, Gruner DS 2013. Microbial symbionts shape the sterol profile of the xylem-feeding woodwasp, Sirex noctilio. J. Chem. Ecol. 39:129–39
    [Google Scholar]
  133. 133. 
    Thummel CS, Chory J. 2002. Steroid signaling in plants and insects: common themes, different pathways. Genes Dev 16:3113–29
    [Google Scholar]
  134. 134. 
    Tohidi-Esfahani D, Graham LD, Hannan GN, Simpson AM, Hill RJ 2011. An ecdysone receptor from the pentatomomorphan, Nezara viridula, shows similar affinities for moulting hormones makisterone A and 20-hydroxyecdysone. Insect Biochem. Mol. Biol. 41:77–89
    [Google Scholar]
  135. 135. 
    Ugine TA, Krasnoff SB, Grebenok RJ, Behmer ST, Losey JE 2019. Prey nutrient content creates omnivores out of predators. Ecol. Lett. 22:275–83Demonstrates that sterol nutrition steers predators to omnivory.
    [Google Scholar]
  136. 136. 
    van der Horst DJ, van Hoof D, van Marrewijk WJ, Rodenburg KW 2002. Alternative lipid mobilization: the insect shuttle system. Mol. Cell. Biochem. 239:113–19
    [Google Scholar]
  137. 137. 
    Van Hoof D, Rodenburg KW, Van der Horst DJ 2002. Insect lipoprotein follows a transferrin-like recycling pathway that is mediated by the insect LDL receptor homologue. J. Cell Sci. 115:4001–12
    [Google Scholar]
  138. 138. 
    Vincent TR, Avramova M, Canham J, Higgins P, Bilkey N et al. 2017. Interplay of plasma membrane and vacuolar ion channels, together with BAK1, elicits rapid cytosolic calcium elevations in Arabidopsis during aphid feeding. Plant Cell 29:1460–79
    [Google Scholar]
  139. 139. 
    Vinci G, Xia X, Veitia RA 2008. Preservation of genes involved in sterol metabolism in cholesterol auxotrophs: facts and hypotheses. PLOS ONE 3:e2883
    [Google Scholar]
  140. 140. 
    Voght SP, Fluegel ML, Andrews LA, Pallanck LJ 2007. Drosophila NPC1b promotes an early step in sterol absorption from the midgut epithelium. Cell Metab 5:195–205The first study in insects showing NPC1b is involved in sterol absorption.
    [Google Scholar]
  141. 141. 
    Wang C, Ma Z, Scott MP, Huang X 2011. The cholesterol trafficking protein NPC1 is required for Drosophila spermatogenesis. Dev. Biol. 351:146–55
    [Google Scholar]
  142. 142. 
    Waterham HR. 2006. Defects of cholesterol biosynthesis. FEBS Lett 580:5442–49
    [Google Scholar]
  143. 143. 
    Willnow TE, Hammes A, Eaton S 2007. Lipoproteins and their receptors in embryonic development: more than cholesterol clearance. Development 134:3239–49
    [Google Scholar]
  144. 144. 
    Xiang Y, Liu Z, Huang X 2010. br regulates the expression of the ecdysone biosynthesis gene npc1. Dev. Biol. 344:800–8
    [Google Scholar]
  145. 145. 
    Xue J, Zhou X, Zhang C-X, Yu L-L, Fan H-W et al. 2014. Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol 15:521–21
    [Google Scholar]
  146. 146. 
    Yamada J, Morisaki M, Iwai K, Hamada H, Sato N, Fujimoto Y 1997. 24-Methyl- and 24-ethyl-16;24(25)-cholesterols as immediate biosynthetic precursors of 24-alkylsterols in higher plants. Tetrahedron 53:877–84
    [Google Scholar]
  147. 147. 
    Yamanaka N, Rewitz KF, O'Connor MB 2013. Ecdysone control of developmental transitions: lessons from Drosophila research. Annu. Rev. Entomol. 58:497–516
    [Google Scholar]
  148. 148. 
    Yang H, Liu X, Zhou F, Hu J, Bhaskar R et al. 2010. Cloning and expression pattern of 3-dehydroecdysone 3β-reductase (3DE 3β-reductase) from the silkworm, Bombyx mori L. Arch. Insect Biochem. Physiol. 76:55–66
    [Google Scholar]
  149. 149. 
    Yun HK, Jouni ZE, Wells MA 2002. Characterization of cholesterol transport from midgut to fat body in Manduca sexta larvae. Insect Biochem. Mol. Biol. 32:1151–58
    [Google Scholar]
  150. 150. 
    Zhang L, Li D, Xu R, Zheng S, He H et al. 2014. Structural and functional analyses of a sterol carrier protein in Spodoptera litura. PLOS ONE 9:e81542
    [Google Scholar]
  151. 151. 
    Zhang L, Reed R. 2017. A practical guide to CRISPR/Cas9 genome editing in Lepidoptera. bioRxiv130344
    [Google Scholar]
  152. 152. 
    Zheng J-C, Sun S-L, Yue X-R, Liu T-X, Jing X 2018. Phylogeny and evolution of the cholesterol transporter NPC1 in insects. J. Insect Physiol. 107:157–66Illustrates the evolution of insect NPC1 and the loss of NPC1b in some linages.
    [Google Scholar]
  153. 153. 
    Zhuang M, Oltean DI, Gómez I, Pullikuth AK, Soberón M et al. 2002. Heliothis virescens and Manduca sexta lipid rafts are involved in Cry1A toxin binding to the midgut epithelium and subsequent pore formation. J. Biol. Chem. 277:13863–72
    [Google Scholar]
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