Skip to main content
SpringerLink
Log in

Lipids in Insect Oocytes: From the Storage Pathways to Their Multiple Functions

  • Chapter
  • First Online:
Oocytes

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 63))

Abstract

In insect physiology, the mechanisms involved in the buildup and regulation of yolk proteins in developing oocytes have been thoroughly researched during the last three decades. Comparatively, the study of lipid metabolism in oocytes had received less attention. The importance of this issue lies in the fact that lipids make up to 40% of the dry weight of an insect egg, being the most important supply of energy for the developing embryo. Since the oocyte has a very limited capacity to synthesize lipids de novo, most of the lipids in the mature eggs arise from the circulation. The main lipid carriers in the insect circulatory system are the lipoproteins lipophorin and vitellogenin. In some species, the endocytosis of lipophorin and vitellogenin may account for about 10% of the lipids present in mature eggs. Thus, most of the lipids are transferred by a lipophorin-mediated pathway, in which the lipoprotein unloads its lipid cargo at the surface of oocytes without internalization. This chapter recapitulates the current status on lipid storage and its utilization in insect oocytes and discusses the participation of key factors including lipoproteins, transfer proteins, lipolytic enzymes, and dynamic organelles such as lipid droplets. The new findings in the field of lipophorin receptors are presented in the context of lipid accumulation during egg maturation, and the roles of lipids beyond energy source are summarized from the perspective of oogenesis and embryogenesis. Finally, prospective and fruitful areas of future research are suggested.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

α-ATPase:

α subunit of the F1FO adenosine triphosphate synthase complex

apoA-I:

apolipoprotein A-I

apoLp-I:

apolipophorin I

apoLp-II:

apolipophorin II

ATPase:

F1FO adenosine triphosphate synthase

β-ATPase:

β subunit of the F1FO adenosine triphosphate synthase complex

bHLH-PAS:

basic helix-loop-helix Per/Arnt/Sim

CaM:

calmodulin

COX:

cyclooxygenases

DAG:

diacylglycerol

DGAT:

acyl-CoA:diacylglycerol O-acyltransferase

EcR:

ecdysone receptor

FAs:

fatty acids

FFAs:

free fatty acids

GPAT:

glycerol-3-phosphate acyltransferase

HCs:

hydrocarbons

HDL:

high-density lipoproteins

HDLp:

high-density lipophorin

IDL:

intermediate-density lipoproteins

IP2 :

phosphatidylinositol 4,5-biphosphate

IP3 :

inositol 1,4,5-trisphosphate

JH:

juvenile hormones

LA:

LDLR class A ligand-binding domain

LDL:

low-density lipoproteins

LDLp:

low-density lipophorin

LDLR:

low-density lipoprotein receptor

LOX:

lipoxygenases

LPL:

lipoprotein lipase

LpR:

lipophorin receptor

LSD-1:

lipid storage droplet 1

LSD-2:

lipid storage droplet 2

LTP:

lipid transfer particle

MAG:

monoacylglycerol

Met:

Methoprene-tolerant

mVg:

microvitellogenin

PGs:

prostaglandins

PLC:

phospholipase C

PLs:

phospholipids

SCRB15:

scavenger receptor class B member 15

SREBP:

sterol regulatory element-binding protein

TAG:

triacylglycerol

TOR:

target of rapamycin

USP:

ultraspiracle

VgR:

vitellogenin receptor

VHDLp:

very high-density lipophorin

VLDL:

very low-density lipoproteins

YPPs:

yolk protein precursors

YPs:

yolk polypeptides

References

  • Aguirre SA, Fruttero LL, Leyria J, Defferrari MS, Pinto PM, Settembrini BP, Rubiolo ER, Carlini CR, Canavoso LE (2011) Biochemical changes in the transition from vitellogenesis to follicular atresia in the hematophagous Dipetalogaster maxima (Hemiptera: Reduviidae). Insect Biochem Mol Biol 41:832–841

    Article  CAS  PubMed  Google Scholar 

  • Aguirre SA, Pons P, Settembrini BP, Arroyo D, Canavoso LE (2013) Cell death mechanisms during follicular atresia in Dipetalogaster maxima, a vector of Chagas’ disease (Hemiptera: Reduviidae). J Insect Physiol 59:532–541

    Article  CAS  PubMed  Google Scholar 

  • Alves-Bezerra M, Gondim KC (2012) Triacylglycerol biosynthesis occurs via the glycerol-3-phosphate pathway in the insect Rhodnius prolixus. Biochim Biophys Acta 1821:1462–1471

    Article  CAS  PubMed  Google Scholar 

  • Alves-Bezerra M, De Paula IF, Medina JM, Silva-Oliveira G, Medeiros JS, Gäde G, Gondim KC (2016) Adipokinetic hormone receptor gene identification and its role in triacylglycerol metabolism in the blood-sucking insect Rhodnius prolixus. Insect Biochem Mol Biol 69:51–60

    Article  CAS  PubMed  Google Scholar 

  • Andries K, Verhasselt P, Guillemont J, Göhlmann HW, Neefs JM, Winkler H, Van Gestel J, Timmerman P, Zhu M, Lee E (2005) A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307:223–227

    Article  CAS  PubMed  Google Scholar 

  • Angel-Dapa MA, Rodríguez-Jaramillo C, Cáceres-Martínez CJ, Saucedo PE (2010) Changes in lipid content of oocytes of the penshell Atrina mauraas a criterion of gamete development and quality: a study of histochemistry and digital image analysis. J Shellfish Res 29:407–413

    Article  Google Scholar 

  • Arechaga I, Jones PC (2001) Quick guide: ATP synthase. Curr Biol 11:R117

    Article  CAS  PubMed  Google Scholar 

  • Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arrese EL, Saudale FZ, Soulages JL (2014) Lipid droplets as signaling platforms linking metabolic and cellular functions. Lipid Insights 7:7–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Atella GC, Shahabuddin M (2002) Differential partitioning of maternal fatty acid and phospholipid in neonate mosquito larvae. J Exp Biol 205:3623–3630

    CAS  PubMed  Google Scholar 

  • Atella GC, Gondim KC, Machado EA, Medeiros MN, Silva-Neto MA, Masuda H (2005) Oogenesis and egg development in triatomines: a biochemical approach. An Acad Bras Cienc 77:405–430

    Article  CAS  PubMed  Google Scholar 

  • Baker KD, Thummel CS (2007) Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metab 6:257–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barneda D, Christian M (2017) Lipid droplet growth: regulation of a dynamic organelle. Curr Opin Cell Biol 47:9–15

    Article  CAS  PubMed  Google Scholar 

  • Beenakkers AMT, Van der Horst DJ, Van Marrewijk WJA (1981) Role of lipids in energy metabolism. In: Downer RGH (ed) Energy metabolism in insects. Plenum, New York, pp 53–100

    Chapter  Google Scholar 

  • Bellés X (2005) Vitellogenesis directed by juvenile hormone. In: Raikhel AS (ed) Progress in vitellogenesis. Reproductive biology of invertebrates, vol 12, part B. Science Publishers, Enfield, pp 157–197

    Google Scholar 

  • Bellés X, Piulachs MD (2015) Ecdysone signalling and ovarian development in insects: from stem cells to ovarian follicle formation. Biochim Biophys Acta 1849:181–186

    Article  PubMed  CAS  Google Scholar 

  • Benoit JB, Yang G, Krause TB, Patrick KR, Aksoy S, Attardo GM (2011) Lipophorin acts as a shuttle of lipids to the milk gland during tsetse fly pregnancy. J Insect Physiol 57:1553–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi J, Xiang Y, Chen H, Liu Z, Grönke S, Kühnlein RP, Huang X (2012) Opposite and redundant roles of the two Drosophila perilipins in lipid mobilization. J Cell Sci 125:3568–3577

    Article  CAS  PubMed  Google Scholar 

  • Bickel PE, Tansey JT, Welte MA (2009) PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim Biophys Acta 1791:419–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blacklock BJ, Ryan RO (1994) Hemolymph lipid transport. Insect Biochem Mol Biol 24:855–873

    Article  CAS  PubMed  Google Scholar 

  • Briegel H (1990) Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol 36:165–172

    Article  Google Scholar 

  • Brooks RA, Woodruff RI (2004) Calmodulin transmitted through gap junctions stimulates endocytic incorporation of yolk precursors in insect oocytes. Dev Biol 271:339–349

    Article  CAS  PubMed  Google Scholar 

  • Brown MS, Goldstein JL (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232:34–47

    Article  CAS  PubMed  Google Scholar 

  • Brown PT, Herbert P, Woodruff RI (2010) Vitellogenesis in Oncopeltus fasciatus: PLC/IP3, DAG/PK-C pathway triggered by CaM. J Insect Physiol 56:1300–1305

    Article  CAS  PubMed  Google Scholar 

  • Büning J (2006) Ovariole structure supports sistergroup relationship of Neuropterida and Coleoptera. Arthropod Syst Phylogeny 64:115–126

    Google Scholar 

  • Canavoso LE, Wells MA (2001) Role of lipid transfer particle in delivery of diacylglycerol from midgut to lipophorin in larval Manduca sexta. Insect Biochem Mol Biol 31:783–790

    Article  CAS  PubMed  Google Scholar 

  • Canavoso LE, Jouni ZE, Karnas KJ, Pennington JE, Wells MA (2001) Fat metabolism in insects. Annu Rev Nutr 21:23–46

    Article  CAS  PubMed  Google Scholar 

  • Canavoso LE, Yun HK, Jouni ZE, Wells MA (2004) Lipid transfer particle mediates the delivery of diacylglycerol from lipophorin to fat body in larval Manduca sexta. J Lipid Res 45:456–465

    Article  CAS  PubMed  Google Scholar 

  • Cardoso AF, Cres RL, Moura AS, Almeida F, Bijovsky AT (2010) Culex quinquefasciatus vitellogenesis: morphological and biochemical aspects. Mem Inst Oswaldo Cruz 105:254–262

    Article  CAS  PubMed  Google Scholar 

  • Carrasco S, Mérida I (2007) Diacylglycerol, when simplicity becomes complex. Trends Biochem Sci 32:27–36

    Article  CAS  PubMed  Google Scholar 

  • Chen ME, Lewis DK, Keeley LL, Pietrantonio PV (2004) cDNA cloning and transcriptional regulation of the vitellogenin receptor from the imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Insect Mol Biol 13:195–204

    Article  CAS  PubMed  Google Scholar 

  • Cheon HM, Seo SJ, Sun J, Sappington TW, Raikhel AS (2001) Molecular characterization of the VLDL receptor homolog mediating binding of lipophorin in oocyte of the mosquito Aedes aegypti. Insect Biochem Mol Biol 31:753–760

    Article  CAS  PubMed  Google Scholar 

  • Chi SL, Pizzo SV (2006) Cell surface F1FO ATP synthase: a new paradigm? Ann Med 38:429–438

    Article  CAS  PubMed  Google Scholar 

  • Chino H, Downer RGH, Takahashi K (1977) The role of diacylglycerol-carrying lipoprotein I in lipid transport during insect vitellogenesis. Biochim Biophys Acta 487:508–516

    Article  CAS  PubMed  Google Scholar 

  • Chinzei Y, Chino H, Wyatt GR (1981) Purification and properties of vitellogenin and vitellin from Locusta migratoria. Insect Biochem 11:1–7

    Article  CAS  Google Scholar 

  • Ciudad L, Bellés X, Piulachs MD (2007) Structural and RNAi characterization of the German cockroach lipophorin receptor and the evolutionary relationships of lipoprotein receptors. BMC Mol Biol 8:53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 58:1007–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dantuma NP, Van Marrewijk WJA, Wynne HJ, Van der Horst DJ (1996) Interaction of an insect lipoprotein with its binding site at the fat body. J Lipid Res 37:1345–1355

    CAS  PubMed  Google Scholar 

  • Dantuma NP, Pijnenburg MA, Diederen JH, Van der Horst DJ (1997) Developmental down-regulation of receptor-mediated endocytosis of an insect lipoprotein. J Lipid Res 38:254–265

    CAS  PubMed  Google Scholar 

  • Dantuma NP, Potters M, De Winther MPJ, Tensen CP, Kooiman FP, Bogerd J, Van der Horst DJ (1999) An insect homolog of the vertebrate very low density lipoprotein receptor mediates endocytosis of lipophorins. J Lipid Res 40:973–978

    CAS  PubMed  Google Scholar 

  • Davey K (2007) From insect ovaries to sheep red blood cells: a tale of two hormones. J Insect Physiol 53:1–10

    Article  CAS  PubMed  Google Scholar 

  • Di Bartolomeo S, Nazio F, Cecconi F (2010) The role of autophagy during development in higher eukaryotes. Traffic 11:1280–1289

    Article  PubMed  CAS  Google Scholar 

  • Downer RGH, Chino H (1985) Turnover of protein and diacylglycerol components of lipophorin in insect haemolymph. Insect Biochem 15:627–630

    Article  CAS  Google Scholar 

  • Drummond-Barbosa D, Spradling AC (2001) Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev Biol 231:265–278

    Article  CAS  PubMed  Google Scholar 

  • Ducharme NA, Bickel PE (2008) Lipid droplets in lipogenesis and lipolysis. Endocrinology 149:942–949

    Article  CAS  PubMed  Google Scholar 

  • Engelmann F, Mala J (2000) The interactions between juvenile hormone (JH), lipophorin, vitellogenin, and JH esterases in two cockroach species. Insect Biochem Mol Biol 30:793–803

    Article  CAS  PubMed  Google Scholar 

  • Entringer PF, Grillo LA, Pontes EG, Machado EA, Gondim KC (2013) Interaction of lipophorin with Rhodnius prolixus oocytes: biochemical properties and the importance of blood feeding. Mem Inst Oswaldo Cruz 108:836–844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan Y, Chase J, Sevala VL, Schal C (2002) Lipophorin-facilitated hydrocarbon uptake by oocytes in the German cockroach Blatella germanica. J Exp Biol 205:781–790

    CAS  PubMed  Google Scholar 

  • Fan Y, Zurek L, Dykstra M, Schal C (2003) Hydrocarbon synthesis by enzymatically dissociated oenocytes of the abdominal integument of the German cockroach, Blattella germanica. Naturwissenschaften 90:121–126

    CAS  PubMed  Google Scholar 

  • Fernandis AZ, Wenk MR (2007) Membrane lipids as signaling molecules. Curr Opin Lipidol 18:121–128

    Article  CAS  PubMed  Google Scholar 

  • Ferreira CR, Saraiva SA, Catharino RR, Garcia JS, Gozzo FC, Sanvido GB, Santos LF, Lo Turco EG, Pontes JH, Basso AC, Bertolla RP, Sartori R, Guardieiro MM, Perecin F, Meirelles FV, Sangalli JR, Eberlin MN (2010) Single embryo and oocyte lipid fingerprinting by mass spectrometry. J Lipid Res 51:1218–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fongsaran C, Jirakanwisal K, Kuadkitkan A, Wikan N, Wintachai P, Thepparit C, Ubol S, Phaonakrop N, Roytrakul S, Smith DR (2014) Involvement of ATP synthase β subunit in chikungunya virus entry into insect cells. Arch Virol 159:3353–3364

    Article  CAS  PubMed  Google Scholar 

  • Foottit RG, Adler PH (2009) Introduction. In: Foottit RG, Adler HP (eds) Insect biodiversity: science and society, 1st edn. Wiley-Blackwell, Oxford, pp 1–6

    Google Scholar 

  • Fruttero LL, Rubiolo ER, Canavoso LE (2009) Biochemical and cellular characterization of lipophorin-midgut interaction in the hematophagous Panstrongylus megistus (Hemiptera: Reduviidae). Insect Biochem Mol Biol 39:322–331

    Article  CAS  PubMed  Google Scholar 

  • Fruttero LL, Frede S, Rubiolo ER, Canavoso LE (2011) The storage of nutritional resources during vitellogenesis of Panstrongylus megistus (Hemiptera: Reduviidae): the pathways of lipophorin in lipid delivery to developing oocytes. J Insect Physiol 57:475–486

    Article  CAS  PubMed  Google Scholar 

  • Fruttero LL, Demartini DR, Rubiolo ER, Carlini CR, Canavoso LE (2014) β-chain of ATP synthase as a lipophorin binding protein and its role in lipid transfer in the midgut of Panstrongylus megistus (Hemiptera: Reduviidae). Insect Biochem Mol Biol 52:1–12

    Article  CAS  PubMed  Google Scholar 

  • Fruttero LL, Leyria J, Ramos FO, Stariolo R, Settembrini BP, Canavoso LE (2017) The process of lipid storage in insect oocytes: the involvement of β-chain of ATP synthase in lipophorin-mediated lipid transfer in the chagas’ disease vector Panstrongylus megistus (Hemiptera: Reduviidae). J Insect Physiol 96:82–92

    Article  CAS  PubMed  Google Scholar 

  • Galetto L, Bosco D, Balestrini R, Genre A, Fletcher J, Marzachì C (2011) The major antigenic membrane protein of “Candidatus Phytoplasma asteris” selectively interacts with ATP synthase and actin of leafhopper vectors. PLoS One 6:e22571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Go GW, Mani A (2012) Low-density lipoprotein receptor (LDLR) family orchestrates cholesterol homeostasis. Yale J Biol Med 85:19–28

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein JL, Brown MS (2009) The LDL receptor. Arterioscler Thromb Vasc Biol 29:431–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gondim KC, Wells MA (2000) Characterization of lipophorin binding to the midgut of larval Manduca sexta. Insect Biochem Mol Biol 30:405–413

    Article  CAS  PubMed  Google Scholar 

  • Gopalapillai R, Kadono-Okuda K, Tsuchida K, Yamamoto K, Nohata J, Ajimura M, Mita K (2006) Lipophorin receptor of Bombyx mori: cDNA cloning, genomic structure, alternative splicing, and isolation of a new isoform. J Lipid Res 47:1005–1013

    Article  CAS  PubMed  Google Scholar 

  • Guo JY, Dong SZ, Ye GY, Li K, Zhu JY, Fang Q, Hu C (2011) Oosorption in the endoparasitoid, Pteromalus puparum. J Insect Sci 11:90

    PubMed  PubMed Central  Google Scholar 

  • Hagedorn HH (1985) The role of ecdysteroids in reproduction. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, Biochemistry and pharmacology, vol 8. Pergamon Press, Oxford, pp 205–261

    Google Scholar 

  • Harizi H, Corcuff JB, Gualde N (2008) Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol Med 14:461–469

    Article  CAS  PubMed  Google Scholar 

  • Havel RJ (1987) Lipid transport function of lipoproteins in blood plasma. Am J Physiol 253:E1–E5

    CAS  PubMed  Google Scholar 

  • Horne I, Haritos VS, Oakeshott JG (2009) Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem Mol Biol 39:547–567

    Article  CAS  PubMed  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    Article  CAS  PubMed  Google Scholar 

  • Huebner E, Anderson E (1972a) A cytological study of the ovary of Rhodnius prolixus. I. The ontogeny of the follicular epithelium. J Morphol 136:459–493

    Article  CAS  PubMed  Google Scholar 

  • Huebner E, Anderson E (1972b) A cytological study of the ovary of Rhodnius prolixus. II. Oocyte differentiation. J Morphol 137:385–415

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Yasuda A, Sonobe H (2008) Synthesis and phosphorylation of ecdysteroids during ovarian development in the silkworm, Bombyx mori. Zoolog Sci 25:721–727

    Article  CAS  PubMed  Google Scholar 

  • Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58:181–204

    Article  CAS  PubMed  Google Scholar 

  • Jindra M, Bellés X, Shinoda T (2015) Molecular basis of juvenile hormone signaling. Curr Opin Insect Sci 11:39–46

    Article  PubMed  Google Scholar 

  • Jouni ZE, Takada N, Gazard J, Maekawa H, Wells MA, Tsuchida K (2003) Transfer of cholesterol and diacylglycerol from lipophorin to Bombyx mori ovarioles in vitro: role of the lipid transfer particle. Insect Biochem Mol Biol 33:145–153

    Article  CAS  PubMed  Google Scholar 

  • Juárez MP (1994) Hydrocarbon biosynthesis in Triatoma infestans eggs. Arch Insect Biochem Physiol 25:193–206

    Article  PubMed  Google Scholar 

  • Kawooya JK, Law JH (1988) Role of lipophorin in lipid transport to the insect egg. J Biol Chem 263:8748–8753

    CAS  PubMed  Google Scholar 

  • Kawooya JK, Osir EO, Law JH (1988) Uptake of the major hemolymph lipoprotein and its transformation in the insect egg. J Biol Chem 263:8740–8747

    CAS  PubMed  Google Scholar 

  • Kory N, Farese RV, Walther TC (2016) Targeting fat: mechanisms of protein localization to lipid droplets. Trends Cell Biol 26:535–546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kühnlein RP (2011) The contribution of the Drosophila model to lipid droplet research. Prog Lipid Res 50:348–356

    Article  PubMed  CAS  Google Scholar 

  • Lagueux M, Hoffmann JA (1984) Ecdysteroids in ovaries and embryos of Locusta migratoria. In: Hoffman JA, Porchet M (eds) Biosynthesis, metabolism and mode of actions of invertebrates hormones. Springer, Berlin, pp 168–180

    Chapter  Google Scholar 

  • Law JH, Wells MA (1989) Insects as biochemical models. J Biol Chem 264:16335–16338

    CAS  PubMed  Google Scholar 

  • Leyria J, Fruttero LL, Aguirre SA, Canavoso LE (2014) Ovarian nutritional resources during the reproductive cycle of the hematophagous Dipetalogaster maxima (Hemiptera: Reduviidae): focus on lipid metabolism. Arch Insect Biochem Physiol 87:148–163

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Thiel K, Thul PJ, Beller M, Kühnlein RP, Welte MA (2012) Lipid droplets control the maternal histone supply of Drosophila embryos. Curr Biol 22:2104–2113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin X, Kim YA, Lee BL, Söderhäll K, Söderhäll I (2009) Identification and properties of a receptor for the invertebrate cytokine astakine, involved in hematopoiesis. Exp Cell Res 315:1171–1180

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Huang X (2013) Lipid metabolism in Drosophila: development and disease. Acta Biochim Biophys Sin (Shanghai) 45:44–50

    Article  CAS  Google Scholar 

  • Liu H, Ryan RO (1991) Role of lipid transfer particle in transformation of lipophorin in insect oocytes. Biochim Biophys Acta 1085:112–118

    Article  CAS  PubMed  Google Scholar 

  • Lone AM, Tasken K (2013) Proinflammatory and immunoregulatory roles of eicosanoids in T cells. Front Immunol 4:130

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu K, Shu Y, Zhou J, Zhang X, Zhang X, Chen M, Yao Q, Zhou Q, Zhang W (2015) Molecular characterization and RNA interference analysis of vitellogenin receptor from Nilaparvata lugens (Stål). J Insect Physiol 73:20–29

    Article  CAS  PubMed  Google Scholar 

  • Lu K, Chen X, Liu WT, Zhang XY, Chen MX, Zhou Q (2016) Nutritional signaling regulates vitellogenin synthesis and egg development through juvenile hormone in Nilaparvata lugens (Stål). Int J Mol Sci 17:269

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Machado EA, Atella GC, Gondim KC, de Souza W, Masuda H (1996) Characterization and immunocytochemical localization of lipophorin binding sites in the oocytes of Rhodnius prolixus. Arch Insect Biochem Physiol 31:185–196

    Article  CAS  PubMed  Google Scholar 

  • Machado E, Swevers L, Sdralia N, Medeiros MN, Mello FG, Iatrou K (2007) Prostaglandin signaling and ovarian follicle development in the silkmoth, Bombyx mori. Insect Biochem Mol Biol 37:876–885

    Article  CAS  PubMed  Google Scholar 

  • Majerowicz D, Calderón-Fernández GM, Alves-Bezerra M, De Paula IF, Cardoso LS, Juárez MP, Atella GC, Gondim KC (2017) Lipid metabolism in Rhodnius prolixus: lessons from the genome. Gene 596:27–44

    Article  CAS  PubMed  Google Scholar 

  • Makki R, Cinnamon E, Gould AP (2014) The development and functions of oenocytes. Annu Rev Entomol 59:405–425

    Article  CAS  PubMed  Google Scholar 

  • McCall K (2004) Eggs over easy: cell death in the Drosophila ovary. Dev Biol 274:3–14

    Article  CAS  PubMed  Google Scholar 

  • Medeiros MN, Oliveira DMP, Paiva-Silva GO, Silva-Neto MAC, Romero A, Bozza M, Masuda H, Machado EA (2002) The role of eicosanoids on Rhodnius heme-binding protein (RHBP) endocytosis by Rhodnius prolixus ovaries. Insect Biochem Mol Biol 32:537–545

    Article  CAS  PubMed  Google Scholar 

  • Medeiros MN, Mendonça LH, Hunter AL, Paiva-Silva GO, Mello FG, Henze IP, Masuda H, Maya-Monteiro CM, Machado EA (2004) The role of lipoxygenase products on the endocytosis of yolk proteins in insects: participation of cAMP. Arch Insect Biochem Physiol 55:178–187

    Article  CAS  PubMed  Google Scholar 

  • Meier T, Faraldo-Gomez J, Börsch B (2011) ATP synthase-a paradigmatic molecular machine. In: Frank J (ed) Molecular machines in biology. Cambridge University Press, Cambridge, pp 208–238

    Chapter  Google Scholar 

  • Miura K, Oda M, Makita S, Chinzei Y (2005) Characterization of the Drosophila Methoprene-tolerant gene product. FEBS J 272:1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Negishi M, Sugimoto Y, Ichikawa A (1995) Molecular mechanisms of diverse actions of prostanoid receptors. Biochim Biophys Acta 1259:109–120

    Article  PubMed  Google Scholar 

  • Nelson DR, Hines H, Stay B (2004) Methyl-branched hydrocarbons, major components of the waxy material coating the embryos of the viviparous cockroach Diploptera punctata. Comp Biochem Physiol B Biochem Mol Biol 138:265–276

    Article  PubMed  CAS  Google Scholar 

  • Niwa R, Niwa YS (2014) Enzymes for ecdysteroid biosynthesis: their biological functions in insects and beyond. Biosci Biotechnol Biochem 78:1283–1292

    Article  CAS  PubMed  Google Scholar 

  • Nomura DK, Casida JE (2016) Lipases and their inhibitors in health and disease. Chem Biol Interact 259:211–222

    Article  CAS  PubMed  Google Scholar 

  • Paingankar MS, Gokhale MD, Deobagkar DN (2010) Dengue-2-virus-interacting polypeptides involved in mosquito cell infection. Arch Virol 155:1453–1461

    Article  CAS  PubMed  Google Scholar 

  • Parra-Peralbo E, Culi J (2011) Drosophila lipophorin receptors mediate the uptake of neutral lipids in oocytes and imaginal disc cells by an endocytosis independent mechanism. PLoS Genet 7:e1001297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pennington JE, Wells MA (2002) Triacylglycerol-rich lipophorins are found in the dipteran infraorder Culicomorpha, not just in mosquitoes. J Insect Sci 2:15

    PubMed  PubMed Central  Google Scholar 

  • Pistillo D, Manzi A, Tino A, PiloBoyl P, Graziani F, Malva C (1998) The Drosophila melanogaster lipase homologs: a gene family with tissue and developmental specific expression. J Mol Biol 276:877–855

    Article  CAS  PubMed  Google Scholar 

  • Raikhel AS (2005) Vitellogenesis of disease vectors, from physiology to genes. In: Marquardt WC (ed) Biology of disease vectors. Elsevier, Academic Press, London, pp 329–346

    Google Scholar 

  • Raikhel AS, Dhadialla TS (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37:217–225

    Article  CAS  PubMed  Google Scholar 

  • Raikhel AS, Brown M, Belles X (2005) Endocrine control of reproductive processes. In: Gilbert L, Gill S, Iatrou K (eds) Comprehensive molecular insect science. Elsevier Press, Oxford, pp 433–491

    Chapter  Google Scholar 

  • Remaley AT, Rifai N, Russell Warnick G (2015) Lipids, Lipoproteins, apolipoproteins and other cardiac risk factors. In: Burtis CA, Bruns DE (eds) Fundamentals of clinical chemistry and molecular diagnostics, 7th edn. Saunders, St. Louis, pp 338–411

    Google Scholar 

  • Riddiford LM (2008) Juvenile hormone action: a 2007 perspective. J Insect Physiol 54:895–901

    Article  CAS  PubMed  Google Scholar 

  • Riddiford LM, Cherbas A, Truman W (2000) Ecdysone receptors and their biological actions. Vitam Horm 60:1–73

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Vázquez M, Vaquero D, Parra-Peralbo E, Mejía-Morales JE, Culi J (2015) Drosophila lipophorin receptors recruit the lipoprotein ltp to the plasma membrane to mediate lipid uptake. PLoS Genet 11:e1005356

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy-Zokan EM, Cunningham CB, Hebb LE, McKinney EC, Moore AJ (2015) Vitellogenin and vitellogenin receptor gene expression is associated with male and female parenting in a subsocial insect. Proc Biol Sci 282:20150787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ryan RO, Van der Horst DJ (2000) Lipid transport biochemistry and its role in energy production. Annu Rev Entomol 45:233–260

    Article  CAS  PubMed  Google Scholar 

  • Ryan RO, Wells MA, Law JH (1986) Lipoprotein interconversions in an insect, Manduca sexta. Evidence for a lipid transfer factor in the hemolymph. J Biol Chem 261:563–568

    CAS  PubMed  Google Scholar 

  • Santos R, Rosas-Oliveira R, Saraiva FB, Majerowicz D, Gondim KC (2011) Lipid accumulation and utilization by oocytes and eggs of Rhodnius prolixus. Arch Insect Biochem Physiol 77:1–16

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Ott U, Lynch JA (2016) Emerging developmental genetic model systems in holometabolous insects. Curr Opin Genet Dev 39:116–128

    Article  CAS  PubMed  Google Scholar 

  • Sevala V, Shu S, Ramaswamy SB, Schal C (1999) Lipophorin of female Blattella germanica (L.): characterization and relation to hemolymph titers of juvenile hormone and hydrocarbons. J Insect Physiol 45:431–441

    Article  CAS  PubMed  Google Scholar 

  • Shao W, Espenshade PJ (2012) Expanding roles for SREBP in metabolism. Cell Metab 16:414–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shirk PD, Perera OP (1998) 5′ coding region of the follicular epithelium yolk polypeptide 2 cDNA in the moth, Plodia interpunctella, contains an extended coding region. Arch Insect Biochem Physiol 39:98–108

    Article  CAS  PubMed  Google Scholar 

  • Sieber MH, Spradling AC (2015) Steroid signaling establishes a female metabolic state and regulates SREBP to control oocyte lipid accumulation. Curr Biol 25:993–1004

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Cuervo AM (2011) Autophagy in the cellular balance. Cell Metabolism 13:495–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458:1131–1135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snigirevskaya ES, Raikhel AS (2005) Receptor-mediated endocytosis of yolk proteins in insect oocytes. In: Raikhel AS (ed) Progress in vitellogenesis. Reproductive biology of invertebrates, vol 12, part B. Adiyodi AG, Adiyodi RG (eds) Science Publishers, Enfield, pp 198–227

    Google Scholar 

  • Soulages JL, Firdaus SJ, Hartson S, Chen X, Howard AD, Arrese EL (2012) Developmental changes in the protein composition of Manduca sexta lipid droplets. Insect Biochem Mol Biol 42:305–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spracklen AJ, Kelpsch DJ, Chen X, Spracklen CN, Tootle TL (2014) Prostaglandins temporally regulate cytoplasmic actin bundle formation during Drosophila oogenesis. Mol Biol Cell 25:397–411

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stanley D (2006) Prostaglandins and other eicosanoids in insects: biological significance. Annu Rev Entomol 51:25–44

    Article  CAS  PubMed  Google Scholar 

  • Stanley D, Kim Y (2011) Prostaglandins and their receptors in insect biology. Front Endocrinol (Lausanne) 2:105

    Google Scholar 

  • Stanley DW, Nor Aliza AR, Tunaz H, Putnam SM, Park Y, Bedick JC (2002) FORUM Eicosanoids in insect biology. Neotrop Entomol 31:341–350

    Article  CAS  Google Scholar 

  • Stanley D, Haas E, Miller J (2012) Eicosanoids: exploiting insect immunity to improve biological control programs. Insects 3:492–510

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun J, Hiraoka T, Dittmer NT, Cho K-H, Raikhel AS (2000) Lipophorin as a yolk protein precursor in the mosquito, Aedes aegypti. Insect Biochem Mol Biol 30:1161–1171

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M, Shinohara Y, Ohsaki Y, Fujimoto T (2011) Lipid droplets: size matters. J Electron Microsc (Tokyo) 1:S101–S116

    Article  CAS  Google Scholar 

  • Swevers L, Raikhel AS, Sappington TW, Shirk P, Iatrou K (2005) Vitellogenesis and post-vitellogenic maturation of the insect ovarian follicle. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, Reproduction and development, vol 1. Elsevier, Pergamon, pp 87–155

    Chapter  Google Scholar 

  • Takeuchi N, Chino H (1993) Lipid transfer particle in the hemolymph of the American cockroach: evidence for its capacity of transfer hydrocarbons between lipophorin particles. J Lipid Res 34:543–551

    CAS  PubMed  Google Scholar 

  • Telfer WH (1979) Sulfate and glucosamine labelling of the intercellular matrix in vitellogenic follicles of a moth. Wilehm Roux Arch Dev Biol 185:347–362

    Article  CAS  PubMed  Google Scholar 

  • Telfer WH, Huebner E, Smith DS (1982) The cell biology of vitellogenic follicles in Hyalophora and Rhodnius. In: King RC, Akai H (eds) Insect ultrastructure, vol 1. Plenum, New York, pp 118–149

    Chapter  Google Scholar 

  • Thiam AR, Farese Jr RV, Walther TC (2013) The biophysics and cell biology of lipid droplets. Nat Rev Mol Cell Biol 14:775–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tootle TL, Williams D, Hubb A, Frederick R, Spradling A (2011) Drosophila eggshell production: identification of new genes and coordination by Pxt. PLoS One 6:e19943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Troy S, Anderson WA, Spielman A (1975) Lipid content of maturing ovaries of Aedes aegypti mosquitoes. Comp Biochem Physiol B 50:457–461

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida K, Sakudoh T (2015) Recent progress in molecular genetic studies on the carotenoid transport system using cocoon-color mutants of the silkworm. Arch Biochem Biophys 572:151–157

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida K, Wells MA (1990) Isolation and characterization of a lipoprotein receptor from the fat body of an insect, Manduca sexta. J Biol Chem 265:5761–5767

    CAS  PubMed  Google Scholar 

  • Tufail M, Takeda M (2008) Molecular characteristics of insect vitellogenins. J Insect Physiol 54:1447–1458

    Article  CAS  PubMed  Google Scholar 

  • Tufail M, Takeda M (2009) Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatory mechanisms. J Insect Physiol 55:87–103

    Article  CAS  PubMed  Google Scholar 

  • Tufail M, Raikhel AS, Takeda M (2005) Biosynthesis and processing of insect vitellogenins. In: Raikhel AS (ed) Progress in vitellogenesis. Reproductive biology of invertebrates, vol 12, part B. Adiyodi AG, Adiyodi RG (eds) Science Publishers, Enfield, pp 1–32

    Google Scholar 

  • Tufail M, Nagaba Y, Elgendy AM, Takeda M (2014) Regulation of vitellogenin genes in insects. Entomol Science 17:269–282

    Article  Google Scholar 

  • Tulenko TN, Sumner AE (2002) The physiology of lipoproteins. J Nucl Cardiol 9:638–649

    Article  PubMed  Google Scholar 

  • Ugur B, Chen K, Bellen HJ (2016) Drosophila tools and assays for the study of human diseases. Dis Model Mech 9:235–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyay SK, Singh H, Dixit S, Mendu V, Verma PC (2016) Molecular characterization of vitellogenin and vitellogenin receptor of Bemisia tabaci. PLoS One 11:e0155306

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Antwerpen R, Law JH (1992) Lipophorin lipase from the yolk of Manduca sexta eggs: identification and partial characterization. Arch Insect Biochem Physiol 20:1–12

    Article  PubMed  Google Scholar 

  • Van Antwerpen R, Salvador K, Tolman K, Gentry C (1998) Uptake of lipids by developing oocytes of the hawkmoth, Manduca sexta. The possible role of lipoprotein lipase. Insect Biochem Mol Biol 28:399–408

    Article  PubMed  Google Scholar 

  • Van Antwerpen R, Pham DQ-D, Ziegler R (2005) Accumulation of lipids in insect oocytes. In: Raikhel AS (ed) Progress in vitellogenesis. Reproductive biology of invertebrates, vol 12, part B. Adiyodi AG, Adiyodi RG (eds) Science Publishers, Enfield pp 265–287

    Google Scholar 

  • Van der Horst DJ, Rodenburg KW (2010a) Lipoprotein assembly and function in an evolutionary perspective. BioMol Concepts 1:165–183

    PubMed  Google Scholar 

  • Van der Horst DJ, Rodenburg KW (2010b) Locust flight activity as a model for hormonal regulation of lipid mobilization and transport. J Insect Physiol 56:844–853

    Article  PubMed  CAS  Google Scholar 

  • Van der Horst DJ, Roosendaal SD, Rodenburg KW (2009) Circulatory lipid transport: lipoprotein assembly and function from an evolutionary perspective. Mol Cell Biochem 326:105–119

    Article  CAS  PubMed  Google Scholar 

  • Van Handel E (1993) Fuel metabolism of the mosquito (Culex quinquefasciatus) embryo. J Insect Physiol 39:831–833

    Article  Google Scholar 

  • Van Heusden MC, Law JH (1989) An insect lipid transfer particle promotes lipid loading from fat body to lipoprotein. J Biol Chem 264(29):17287–17292

    PubMed  Google Scholar 

  • Van Hoof D, Rodenburg KW, Van der Horst DJ (2005) Receptor-mediated endocytosis and intracellular trafficking of lipoproteins and transferrin in insect cells. Insect Biochem Mol Biol 35:117–128

    Article  PubMed  CAS  Google Scholar 

  • Vantourout P, Radojkovic C, Lichtenstein L, Pons V, Champagne E, Martinez LO (2010) Ecto-F1-ATPase: a moonlighting protein complex and an unexpected apoA-I receptor. World J Gastroenterol 16:5925–5935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walker JE (1998) ATP synthesis by rotary catalysis. Angew Chem Int Ed 37:2309–2319

    Article  Google Scholar 

  • Wang Y, Telfer WH (1996) Cyclic nucleotide-induced termination of vitellogenin uptake by Hyalophora cecropia follicles. Insect Biochem Mol Biol 26:85–94

    Article  CAS  PubMed  Google Scholar 

  • Wang SF, Zhu J, Martin D, Raikhel AS (2005) Regulation of vitellogenin gene expression by ecdysteroids. In: Raikhel AS (ed) Progress in vitellogenesis. Reproductive biology of invertebrates, vol 12, part B. Adiyodi AG, Adiyodi RG (eds) Science Publishers, Enfield, pp 70–93

    Google Scholar 

  • Welte MA (2015) As the fat flies: the dynamic lipid droplets of Drosophila embryos. Biochim Biophys Acta 1851:1156–1185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiemerslage LJ (1976) Lipid droplets formation during vitellogenesis in the cecropia moth. J Insect Physiol 22:41–50

    Article  CAS  Google Scholar 

  • Wilson TG, Fabian JA (1986) Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev Biol 118:190–201

    Article  CAS  PubMed  Google Scholar 

  • Wyatt GR, Braun RP, Zhang J (1996) Priming effect in gene activation by juvenile hormone in locust fat body. Arch Insect Biochem Physiol 32:633–640

    Article  CAS  Google Scholar 

  • Ximenes AA, Oliveira GA, Bittencourt-Cunha P, Tomokyo M, Leite DB, Folly E, Golodne DM, Atella GC (2008) Purification, partial characterization and role in lipid transport to developing oocytes of a novel lipophorin from the cowpea weevil, Callosobruchus maculatus. Braz J Med Biol Res 41:18–25

    Article  CAS  PubMed  Google Scholar 

  • Yamada R, Sonobe H (2003) Purification, kinetic characterization and molecular cloning of a novel enzyme ecdysteroid phosphate phosphatase. J Biol Chem 278:26365–26373

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Galea A, Sytnyk V, Crossley M (2012) Controlling the size of lipid droplets: lipid and protein factors. Curr Opin Cell Biol 24:509–516

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama H, Yokoyama T, Yuasa M, Fujimoto H, Sakudoh T, Honda N, Fugo H, Tsuchida K (2013) Lipid transfer particle from the silkworm, Bombyx mori, is a novel member of the apoB/large lipid transfer protein family. J Lipid Res 54:2379–2390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalewska M, Kochman A, Estève JP, Lopez F, Chaoui K, Susini C, Ozyhar A, Kochman M (2009) Juvenile hormone binding protein traffic. Interaction with ATP synthase and lipid transfer proteins. Biochim Biophys Acta 1788:1695–1705

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Ma L, Xiao H, Xie B, Smagghe G, Guo Y, Liang G (2015) Molecular characterization and function analysis of the vitellogenin receptor from the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae). PLoS One 11:e0155785

    Article  CAS  Google Scholar 

  • Ziegler R (1997) Lipid synthesis by ovaries and fat body of Aedes aegypti (Diptera: Culicidae). Eur J Entomol 94:385–391

    CAS  Google Scholar 

  • Ziegler R, Van Antwerpen R (2006) Lipid uptake by insect oocytes. Insect Biochem Mol Biol 36:264–272

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Authors thank Dr. B. P. Settembrini and Dr. E. R. Rubiolo for helpful suggestions and critical reading. Unpublished scanning electron micrographs were obtained in collaboration with Dr. B. P. Settembrini.

Funding

Work in the L.E.C. laboratory is supported by grants from SECyT-UNC, FONCyT (PICT 2013-0626), and CONICET (PIP 0159).

Authors’ Contribution

L.L.F., J.L., and L.E.C. wrote the chapter and approved the final version. The authors declare that there is no conflict of interest in regard to the contents of this chapter.

Author information

Authors and Affiliations

  1. Instituto do Cerebro (InsCer). Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, RS, Brazil

    Leonardo L. Fruttero

  2. Departamento de Bioquímica Clínica, Centro de Investigaciones en Bioquímica Clínica e Inmunología (CIBICI-CONICET), Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Córdoba, CP 5000, Argentina

    Jimena Leyria & Lilián E. Canavoso

Authors
  1. Leonardo L. Fruttero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jimena Leyria
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lilián E. Canavoso
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lilián E. Canavoso .

Editor information

Editors and Affiliations

  1. Department of Surgery, The Houston Methodist Hospital, Houston, Texas, USA

    Malgorzata Kloc

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Fruttero, L.L., Leyria, J., Canavoso, L.E. (2017). Lipids in Insect Oocytes: From the Storage Pathways to Their Multiple Functions. In: Kloc, M. (eds) Oocytes. Results and Problems in Cell Differentiation, vol 63. Springer, Cham. https://doi.org/10.1007/978-3-319-60855-6_18

Download citation

Publish with us

Policies and ethics

Search

Navigation