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Keywords:

  • ecdysteroid;
  • endocrine disruptor;
  • juvenile hormone;
  • yolk protein

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

Vitellogenins (Vg) genes code for the major egg yolk protein precursor in insects and many other oviparous species. In insects, the Vg gene is expressed extra-ovarially in the fat body in sex-, tissue- and stage-specific manners. During the reproductive phase, the Vg mRNA is expressed in large quantities, which is then translated, secreted into hemolymph and ultimately taken up by the developing oocytes through receptor-mediated endocytosis. Once sequestered, the Vgs are stored as vitellin (Vn), the main nutritional reserve for the developing embryo. The regulation of Vg genes is directly under the control of hormones at the transcriptional level. Hormones involved in Vg gene transcription are juvenile hormone (JH), ecdysteroids and some neuropeptides. The overall understanding that has emerged is that the insects can be classified, based on the system of hormonal regulation of Vg gene transcription, into three groups: (i) insects (like most of hemipterans) that use only JH for Vg gene transcription; (ii) insects (like dipterans) that need both JH and ecdysteroids for Vg regulation; and (iii) insects like lepidopterans that require JH, ecdysteroids and additional hormones to regulate their reproductive biology. However, why insect species diverge in using different hormones to govern their reproductive physiology remains unclear. The present contribution focuses on the current status of knowledge regarding the regulation of Vg genes in insects. Besides a brief information on biochemical and molecular features, the role of Vg genes as a target of endocrine disruptors will be addressed. Also, the molecular mechanism of Vg gene regulation will be discussed.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

Vitellogenin (Vg) genes code for the major egg yolk protein precursor in insects and many other oviparous species. Insect Vgs are large molecules (∼200 kDa) synthesized extra-ovarially by the fat body in tissue-, sex-, and stage-specific manners, secreted into the hemolymph and then sequestered by competent oocytes by receptor-mediated endocytosis (Raikhel & Dhadialla 1992; Sappington & Raikhel 1998; Snigirevskaya & Raikhel 2005; Tufail & Takeda 2005, 2007, 2009a,b, 1993). In insects, the Vg molecules undergo proteolytic cleavage soon after synthesis in the fat body, and are co- and post-translationally modified. This post-transcriptional processing enables Vg molecules to carry with them the carbohydrates, lipids and other nutrients to the ovaries (see reviews in Raikhel & Dhadialla 1992; Hagedorn et al. 1998; Giorgi et al. 1999; Sappington et al. 2002; Tufail et al. 2005). Once Vg becomes part of the egg yolk, it is stored as vitellin (Vn), the main nutritional reserve for the developing embryo.

In insects, the female-specific hemolymph protein was first identified by Telfer (1954) in Hyalophora cecropia (L.) and it was named “vitellogenin” as the precursor of Vn or yolk protein (YP) by Pan et al. (1969). Later work, however, revealed that Vg expression was not always female-specific as it could be expressed, although in smaller amounts, in males of some species (Engelmann 1979; Trenczek & Engels 1986; Valle 1993; Piulachs et al. 2003), and also that the YPs were expressed in ovaries, in addition to the fat body, as was seen in Cyclorrhapha (Belles 1998, 2005; Giorgi et al. 2005).

In general, insect “yolk proteins” may be categorized into four types: (i) The YPs (like Vgs of most insect species) that are synthesized in the fat body cells in a sex-specific manner and sequestered by the developing oocytes; (ii) YPs that are produced both in the female fat body cells and ovarian follicle cells in a sex-specific manner and are incorporated into developing oocytes (YPs of Cyclorrhapha); (iii) YPs that are synthesized in the ovarian follicle cells and incorporated into the developing oocytes in a sex-specific manner (egg-specific protein in Bombyx mori (L.)); and (iv) YPs that are produced in the fat body cells in a sex non-specific manner and secreted into the hemolymph and internalized by the developing oocytes (such as the 30-kD protein of B. mori).

In this review, we provide our current understanding regarding the regulation of the Vg gene in insects. We will briefly discuss the biochemical and molecular aspects of this important molecule in addition to the role Vg genes as a target of endocrine disruptors in insects. Subsequently, hormonal regulation of Vg biosynthesis in different insect groups, and molecular aspects of Vg gene regulation will be addressed.

Biochemical and molecular aspects of insect vitellogenins

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

In most insects, Vgs are large molecules (∼200 kDa), which are derived from a single Vg gene transcript of 6–7 kbp (Tufail & Takeda 2008) (see Table 1). Vgs are proteolytically processed before secreted into the hemolymph into smaller polypeptides ranging from 50–180 kDa (see reviews: Sappington & Raikhel 1998; Tufail et al. 2005; Tufail & Takeda 2008, 2009c, 2012). These subunit polypeptides are assembled together, following extensive co- and post-translational modifications, and subsequently secreted as big oligomeric phosphoglycolipoproteins (400–600 kDa). Sometimes, Vgs are further cleaved in the ovary as has been observed in the cockroach Leucophaea maderae (F.) (Tufail & Takeda 2002).

Table 1. Vg genes and hormonal specificity identified for their regulation in different insect species
SpeciesAccession no. (DDBJ)Vg (transcript)a identifiedTissueSexStage (method used)HormoneReferences
  1. a

    No of Vg genes identified while known transcript size is given in parentheses. –, data not available; E20, 20-hydroxyecdysone; FB, fat body; JH, Juvenile hormone; Meth, Methoprene; NB, Northern blot analysis; RT-PCR, reverse transcription polymerase chain reaction.

Dictyoptera       
Periplaneta americana-Vg1 AB034804 2 (6.5 kb)FBFemaleAdult (NB)JH IIITufail et al. (2000); A.M. Elgendy, M. Tufail and M. Takeda (unpubl. data, 2008)
Periplaneta americana-Vg2 AB047401     JH IIITufail et al. (2001); A.M. Elgendy, M. Tufail and M. Takeda (unpubl. data, 2008)
Leucophaea maderae-Vg1 AB052640 2 (6.6 kb)FBFemaleAdult (NB)JH/MethTufail and Takeda (2002); Don-Wheeler and Engelmann (1991)
Leucophaea maderae-Vg2 AB194976      Tufail et.al. (2007); Don-Wheeler and Engelmann (1997)
Blattella germanica AJ005115 1 (6.6 kb)FBFemaleAdult (NB)JH IIIComas et al. (1999, 2000)
Hemiptera       
Nilaparvata lugens AB353856 1 (6.8 kb)FBFemaleAdult (NB)JH IIITufail et al. (2010)
Lethocerus deyrollei AB425334 1 (6.5 kb)FBFemaleAdult (NB)JH IIINagaba et al. (2010)
Riptortus clavatusU97272 (6.3 kb)FBFemaleAdult (NB)JH I–II/MethHirai et al. (1998); Shinoda (1996)
Plautia stali-Vg1–3 AB033498-5003 (6.5 kb: Vg1)FBFemaleAdult (NB)Lee et al. (2000a)
Graptopsaltria nigrofuscata AB026848 1 (6.8 kb)FBFemaleAdult (NB)Lee et al. (2000b)
Homalodisca coagulata DQ118408 1W.B Hunter & L.E. Hunnicutt (unpubl. data, 2005)
Coleoptera       
Anthonomus grandis M72980 1 (6.0 kb)FBFemaleAdult (NB)Trewitt et al. (1992)
Hymenoptera       
Athalia rosae AB007850 1 (6.5 kb)FBFemalePupa/adult (NB)Kageyama et al. (1994); Nose et al. (1997)
Pimpla nipponica AF026789 1 (6.0 kb)FBFemaleAdult (NB)Nose et al. (1997)
Apis mellifera AJ517411 1 (5.8 kb)FBFemalePupa/adult (NB)JHPiulachs et al. (2003); Guidugli et al. (2005)
  (5.8 kb) MaleAdult (NB)  
Encarsia formosa AY553878 1Donnell (2004)
Pteromalus puparum EF468683 1FBFemaleLate pupa/adult RT-PCR)Ye et al. (2008)
Solenopsis invicta-Vg1 AF512520 3Lewis et al. (unpubl. data, 2002)
Solenopsis invicta-Vg2 AY941795 H. Tian, B.S. Vinson and C.J. Coates (unpubl. data, 2005)
Solenopsis invicta-Vg3 AY941796 H. Tian, B.S. Vinson and C.J. Coates (unpubl. data, 2005)
Diptera       
Aedes aegypti U02548 5 (6.5 kb)FBFemaleAdult (NB)E20 and JHChen et al. (1994); Romans et al. (1995); Raikhel (1992); Dhadialla & Raikhel (1994)
Anopheles gambiae AF281078 2P.A. Romans (unpubl. data, 2000)
Lepidoptera       
Bombyx mori D13160 1 (5.7 kb)FBFemaleLarva/pupa (NB)20EYano et al. (1994a,b); Tsuchida et al. (1987)
Lymantria dispar U90756 1 (5.5 kb)FBFemaleLarva (NB)20EHiremath and Lehtoma (1997a,b); Fescemyer et al. (1992)
Antheraea pernyiAB049631Liu et al. (2001)
Antheraea yamamai AB055843 1Liu et al. (2006)
Bombyx mandarina AB055845 1Meng et al. (2006)
Actias selene EF523567 1    Yin et al. (2007)
Spodoptera litura ABU68426 1FBFemaleLate pupa/adult (RT-PCR)Shu et al. (2009)
Saturnia japonica AB190809 1Meng et al. (2008)
Samia cynthia AB055844 1Kajiura et al. (unpubl. data, 2001)

The recent molecular data showed that Vg molecules were cleaved in all insect species except Apocrita (higher Hymenoptera) where Vg gene product of ∼180 kDa remains uncleaved (see Tufail & Takeda 2008). However, the Vgs of some hemimetabolous members (like cockroaches and the bean bug Riptortus clavatus Thunberg) are special, cleaved into more than two subunit polypeptides (Hirai et al. 1998; Tufail & Takeda 2002, 2008, 2009c). Instead, the amino acid sequences of yolk protein precursor of Cyclorrhapha (higher Diptera) YPs are quite different from those of other insect Vgs and are also not cleaved.

Moreover, Vgs are members of a larger superfamily of molecules known as large lipid transfer proteins (Babin et al. 1999), and are conserved among organisms as diverged as nematode and vertebrates (Blumenthal & Zucker-Aprison 1987; Spieth et al. 1991; Chen et al. 1997; Sappington et al. 2002; Tufail & Takeda 2008, 2012) as has been shown in our phylogenetic tree (Fig. 1). Our phylogenetic tree constructed based on 60 insect and non-insect Vg sequences reveals that insect Vgs are closer to nematode and arachnid Vgs than vertebrate and crustacean Vgs. Furthermore, the crustacean Vgs form the most distantly related group to all the other Vgs (Fig. 1), and thus possibly reflect the diversification of terrestrial and aquatic lives. The data from some terrestrial crustaceans like Armadirillium vulgare (Latr.) may prove the reality.

figure

Figure 1. Phylogenetic analysis of 60 Vg sequences. A distance analysis of amino acid sequences was performed using CLUSTAL W software and used as input for a neighbor-joining tree construction program MEGA3 (Kumar et al. 2001). Bootstrap values (500 replications) are indicated at each node. Only support values >50% are shown. The scale indicates the distance (number of amino acid substitutions per site). Vg sequences used for phylogenetic analysis were from the following species (accession number in parentheses): Periplaneta americana (Vg1: AB034804; Vg2: AB047401), Leucophaea maderae (Vg1: AB052640; Vg2: AB194976), Blattella germanica (AJ005115), Lethocerus deyrollei (AB425334), Graptopsaltria nigrofuscata (AB026848), Plautia stali (Vg1: AB033498; Vg2: AB033499; Vg3: AB033500), Riptortus clavatus (U97277), Homalodisca coagulata (DQ118408), Nilaparvata lugens (AB353856), Anthonomus grandis (M72980), Tenebrio molitor (AY714212), Athalia rosae (AB007850), Pimpla nipponica (AF026789), Apis mellifera (AJ517411), Encarsia formosa (AY553878), Pteromalus puparum (EF468683), Solenopsis invicta (Vg1: AF512520; Vg2: AY941795; Vg3: AY941796), Aedes aegypti (U02548), Anopheles gambiae (AF281078), Anopheles albimanus (AY691327), Toxorynchites amboinensis (AY691326), Culex pipiens quiquefasciatus (AY691324), Bombyx mori (D13160), Lymantria dispar (U90756), Antheraea pernyi (AB049631), Antheraea yamamai (AB055843), Samia cynthia ricini (AB055844), Bombyx mandarina (AB055845), Saturnia japonica (AB190809), Actias selene (EF523567), Spodoptera litura (EU095334), Caenorhabditis elegans (Vg1: AAB52675; Vg5: AAA83587; Vg6C AAQ91901), Dermacentor variabilis (Vg1: AAW78557; Vg2: ABW82681), Rhipicephalus microplus (ABS88989), Tetranychus urticae-Vg1–4 (AB505063-66), Danio rerio (NP_739573), Gallus gallus (AAA49139), Ichthyomyzon unicuspis (Q91062), Macrobrachium rosenbergii (BAB698831), Pandalus hypsinotus (BAD11098), Cherax quadricarinatus (AAG17936), Metapenaeus ensis (Vg1: AAM48287; Vg2 AAT01139; Vg3 (AAN40700), Marsupenaeus japonicus (BAD98732), Litopenaeus vannamei (AAP76571), Fenneropenaeus merguiensis (AAR88442) and Penaeus mondon (ABB89953).

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As far molecular aspects of insect Vgs are concerned, the sequence comparison of 37 Vg molecules (from 31 insect species) has revealed yet the existence of the usual five particular subdomains of high sequence similarity (data not shown) (see Chen et al. 1997; Sappington & Raikhel 1998; Lee et al. 2000b; Tufail & Takeda 2008). The sequence comparison has also shown a highly conserved motif GL/ICG, the polycysteines conserved at their specific sites, and the DGXR motif that resides 17–19 residues upstream of the GL/ICG in most of the insect species (data not shown). Readers may review, for details, the recently published reviews by the same authors (Tufail et al. 2005; Tufail & Takeda 2008, 2009c, 2012).

Vg genes and their regulation in insects

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

The number of Vg genes varies (one to several) in different species (Table 1) (see review in Tufail & Takeda 2008). In insects, the regulation of Vg gene expression is under hormonal control. We have characterized both at biochemical and molecular levels two Vg genes each of the two cockroach species, Periplaneta americana (L.) and L. maderae (Tufail et al. 2000, 2001, 2005, 2007; Tufail & Takeda 2007, 2008). Multiple Vg genes have also been sequenced from other insect species including Locusta migratoria (R and F) (Wyatt et al. 1984), R. clavatus (Hirai et al. 1998), Plautia stali (Scott) (Lee et al. 2000a), Solenopsis invicta Buren (GeneBank Accession nos AF512520, AY941795 and AY941796) and Aedes aegypti (L.) (Romans et al. 1995) (for more detail see Tufail et al. 2005; Tufail & Takeda 2008). Recently, in silico whole-genome analysis isolated several new Vg gene sequences from several mosquito species including Anopheles albimanus (Wiedemann), Ae. aegypti, Aedes polynesiensis (Marks), Aedes albopictus (Skuse), Ochlerotatus atropalpus (Coquillett), Ochlerotatus triseriatus (Say), Culex pipiens (L.) and Toxorhynchites amboinensis (Doleschall) (Isoe & Hagedorn 2007). Nevertheless, it remains unclear why some insects harbor multiple Vg genes.

In insects, the regulation of Vg genes is directed, as mentioned above, by hormones at the transcriptional level. The sex- and tissue-associated, and hormone-mediated developmental specificities of Vg gene transcription have been reported for many insect species (Table 1) (Bownes 1986; Belles 1998; Tufail et al. 2000, 2010; Tufail & Takeda 2002, 2008, 2009c, 2012; Nagaba et al. 2010). The hormones involved in Vg gene transcription are juvenile hormone (JH), ecdysone (a product of the ovaries) and neuropeptides (Wyatt & Davey 1996; Raikhel et al. 2004; Belles 1998, 2005; Tufail & Takeda 2008). Among them, JH is well documented for its involvement in Vg gene transcription of many insect species (Engelmann 1983; Wyatt & Daevy 1996; Belles 1998, 2005; Tufail & Takeda 2008) (see Table 1). JH is a sesquiterpenoid hormone synthesized and secreted by the corpus allatum (CA). In addition to its well-known role as a (negative) regulator of metamorphosis, JH also plays an important role as a gonadotropin in the adult stage of many insects, where it regulates transcription of the major YP precursor gene Vg. Several forms of JH, like JH 0, JH I, JH II, JH III, hydroxyl JH IIIs, JH bisepoxide3 and JH skipped B3 have been identified (see reviews for details: Goodman & Cusson 2012; Jindra et al. 2013). Among them, JH III (methyl (2E,6E)-10,11-epoxy-3,7,11-trimethyl-2,6-dodecadienoate) is the most commonly involved in Vg regulation, and exists in the vast majority of insect groups. The hormones involved in Vg gene transcription in different insect groups are discussed in detail below.

Vg gene as a target of endocrine disruptors

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

Endocrine disruptors (EDs) are synthetic or naturally occurring chemicals that are present in the environment and interfere with normal endocrine function (Arcand-Hoy & Benson 1998). Recent studies revealed that a number of environmental pollutants (EP) interfered with the normal endocrine physiology of several animals including insects. In milkweed bug Oncopeltus fasciatus (Dallas), for example, cadmium exposure delays ovarian maturation and inhibits vitellogenesis, probably by reduction in Vg gene expression (Cervera et al. 2005, 2006). In another study with Spodoptera litura (F.), lead elicits an important Vg response (Shu et al. 2009). Vg gene has been used as a molecular marker to identify the potential endocrine disruptors both in aquatic vertebrates and aquatic invertebrates. In fish, for example, many EPs have been shown, or are suspected, to have endocrine disrupting potential that may adversely affect the reproductive physiology of fish by directing the Vg expression (Shioda & Wakabayashi 2000).

Recently we have cloned a cDNA encoding Vg and used as a marker to identify the role of ED chemicals (EDCs) in giant water bug Lethocerus deyrollei Vuillefroy, which is dwindling in Japan (Nagaba et al. 2010). Dramatic induction or inhibition of Vg gene expression was detected when diapausing females were injected with EDCs (along with JH III). Among the EDCs tested, 17-β-estradiol and bisphenol A up-regulated the Vg gene expression while 4-t-octylphenol and 4-nonylphenol down-regulated the expression of this gene. These results reveal that EDCs may disrupt the reproductive physiology of L. deyrollei in nature, and thus provide the first warning on potential involvement of EPs in purging this species from the Japanese ecosystem. However, it remains unclear that how EDCs affect the reproductive physiological of this insect species.

Molecular mechanism of Vg gene transcription

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

The regulation of Vg gene transcription depends on the binding of the hormone-receptor complex at hormone responsive elements (HREs) usually located in the upstream regulatory region of the genes (Segraves 1994). These are short-sequence motifs (∼15 bp) that contain elements of palindromic symmetry, direct repeats or inverted repeats represented by multiple copies. The promoter sequences of Vg genes in L. migratoria (Locke et al. 1987) and that of an oothecin gene in P. americana (a JH-controlled gene; Pau 1987) suggested the presence of a possible juvenile hormone responsive elements (JHRE) (Wyatt 1988). This JHRE contains an octanucleotide motif AAGGGTTC, which also occurs in Drosophila heat shock protein (hsp) 27 ecdysteroid response element. Furthermore, in the upstream region of the jhp21 gene of L. migratoria, the partially palindromic 13-nucleotide motif AGGTTCGAGA/TCCT was found in three copies. This motif is also suggestive of hormone responsive elements (HRE), which is similar to the consensus ecdysteroid response element (Jiang et al. 2000). Recently, we have also identified a number of motifs similar to HREs in the promoter regions of P. americana Vg genes (Vg1 and Vg2; accession numbers AB449027 and AB449027, respectively); especially, AGGTCTGAAAGGTC in Vg1 (at position –201) and AGTCACGGAGTC in Vg2 (at position –169) show consensus with the JHRE (A.M. Elgendy, M. Tufail and M. Takeda, unpubl. data, 2008). Using a series of constructs of the promoter sequence of Vg2 with a luciferase assay system, the construct between nucleotides 204 and 144 from the transcription start site with the motif AGTCACGGAGTC induced strong transcription after JH application, suggesting that this could be a response element for the protein(s) involved in JH-induced transcription.

Although the molecular mechanism of JH is not yet clear, several efforts have been made to identify the JH receptor by isolating a protein that binds to radioactively labeled JH or JH analogues. There are currently two candidates proposed for the JH receptor: (i) ultraspiracle (USP), the nuclear receptor; and (ii) methoprene-tolerant (MET), the bHLH-PAS protein family member. The USP model is based on the ability of the receptor to bind with low affinity (dissociation constant, Kd 4 μM) to JH and JH-like ligands (Jones & Jones 2000; Xu et al. 2002). It was reported that JH binds to Drosophila USP to modify its conformation and to induce USP-dependent transcription (Jones & Sharp 1997). Also, yeast two hybrid analyses indicated that JH could promote USP homodimerization. Jones et al. (2001) described that recombinant USP binds to direct repeat 12 (DR12) HRE in gel shift assays, whereas the same DR12 confers enhanced transcriptional JH-responsiveness to a transfected JH esterase core promoter in the transfected cells. The hypothesis that USP may behave as JH receptor either as homodimer or as partner of a hypothetical heterodimer is yet not clear. Indeed, the formation of such dimers explains at least the interaction between JH and ecdysteroid. Experiments with USP mutant Drosophila suggest that loss of USP function disturbs the balance between JH and ecdysone signaling (Hall & Thummel 1998). Given that USP is a mammalian retinoid X receptor (RXR) homolog, it is not surprising that it can heterodimerize with several distinct partners, including Drosophila hormone receptor 38 (DHR38) (Zhou et al. 2000, 2002; Riddiford et al. 2001). Future research in this direction should lead to the identification of the USP ligand and/or coactivator.

The MET model is based on genetic evidence indicating that the methoprene-tolerant gene (Met), when mutated, confers resistance to toxic doses of JH (Pursley et al. 2000; Wilson 2004). Also, Met mutants display reduced intracellular JH binding activity. MET protein is found solely in cell nuclei and have been detected in several tissues, some of which are known as targets of JH. Given that MET belongs to the family of transcriptional regulators, it is plausible that it is involved in JH signaling. However, null Met mutants are completely viable, suggesting that MET may not be a JH receptor. Recently, Met has been shown to bind JH and its mimics with high affinity through a well-conserved hydrophobic pocket within its PAS (Per-Arnt-Sim)-B domain in Tribolium castaneum Herbst (Charles et al. 2011). These workers identify specific amino acid residues responsible for JH binding and demonstrate that the ligand-binding capacity is necessary for interaction of Met with its partner Taiman.

Also, Sheng et al. (2011) have tried to explore the mechanism of JH action in the regulation of Vg gene expression. Injection of bovine insulin or double-stranded RNA targeting the forkhead box transcription factor O (FOXO) gene into previtellogenic, starved or JH-deficient female adults up-regulated Vg mRNA and protein levels, thus implicating the critical role for insulin-like peptide signaling in the regulation of Vg gene transcription and possible cross-talk between JH and insulin-like peptide signaling pathways. These findings suggest that JH functions through insulin-like peptide signaling pathways to regulate Vg gene expression. A recently published review (Jindra et al. (2013) presents potential candidates/partners and their possible role in JH signaling.

Hormonal regulation of Vg gene transcription in different insect groups

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

The hormones involved in Vg gene transcription are JH, ecdyson and neuropeptides (Wyatt & Davey 1996; Belles 1998, 2005; Raikhel et al. 2004; Tufail & Takeda 2008). In general, insects can be classified into three major groups based on the mechanism of hormonal regulation of Vg gene transcription. Group I includes insects that use only JH for Vg gene transcription. In most of the insect species investigated JH is the best-known gonadotropin (Engelmann 1983; Wyatt & Davey 1996; Belles 1998; Raikhel et al. 2004). Group II includes the cases in which regulation of the Vg gene requires ecdysteroid, a product from ovaries (Hagedorn et al. 1975) in addition to the JH (such as Diptera). Group III includes lepidopterans and other insects that require JH, ecdysteroids and additional hormones to regulate their reproductive biology. Hormonal regulation of Vg gene transcription in different insect groups is discussed below.

Dictyoptera

Cockroaches have been classical models for JH-dependent vitellogenesis (Martin 1995, 1996; Don-Wheeler & Engelmann 1997; Comas et al. 2001). In other words, the cockroaches are the first and best known insects where action of JH on Vg gene transcription has been revealed. Most of the information derives from P. americana, L. maderae, Blattella germanica (L.), Nauphoeta cinerea (Olivier) and Diploptera punctata (Eschscholtz) (Engelmann 1983). In P. americana, for example, the ovarian gonotrophic cycles, including both the synthesis and uptake of Vgs, are regulated by JH (see reviews by Engelmann 1983; Wyatt & Davey 1996). Weaver and Edward (1990) have shown that JH is required for Vg synthesis, oocyte growth and ootheca formation in P. americana. Also, we have provided molecular evidence in P. americana that transcription of the two Vg genes (Vg1 and Vg2) (Tufail et al. 2000, 2001; Tufail & Takeda 2008) is activated by JH III and suppressed by 20-hydroxyecdysone (20E) at the transcriptional level in a dose-dependent manner (A.M. Elgendy, M. Tufail and M. Takeda, unpubl. data, 2008).

In B. germanica, transcription of the Vg gene has been shown to start as early as 2 h after the primary stimulation of JH III to allatectomized females (Comas et al. 1999). The growth of terminal oocytes has also been shown to respond to different doses of JH I and analogues in B. germanica (Kunkel 1973). In B. germanica, as in all other cockroaches studied to date, Vg synthesis and cyclic maturation of oocytes depends on JH III (see Schal et al. 1997; Belles 1998 and references therein).

In L. maderae also, Vg synthesis is strictly controlled by JH or its analogues. Vg induction by JH and/or its analogues has been demonstrated even in males and nymphs, although in traces, of some cockroach species including N. cinerea, D. punctata, B. germanica and L. maderae (Don-Wheeler & Engelmann 1991 and references therein). In L. maderae, a JH analogue, methoprene was used for Vg induction in adult females and males. It was reported that Vg precursor is synthesized in the sexually dimorphic fat bodies in the same and stepwise fashion (Don-Wheeler & Engelmann 1997), suggesting again the sole and strong role of JH in Vg gene regulation.

Orthoptera

The regulation of Vg gene transcription depends on JH in several species of grasshoppers and locusts (Engelmann 1983; Wyatt & Davey 1996). The most thorough studies on Vg regulation by JHs, including data on molecular action, have been accomplished in L. migratoria. It has been demonstrated that JH is involved in the transcription of the Vg gene in the female fat body. Vg mRNAs were detected in the fat body and were shown to be induced in response to JH (Chinzei et al. 1982; Chinzei & Wyatt 1985; Zhang et al. 1993). Also, Glinka and Wyatt (1996) have shown that a JH analogue activates the transcription of a gene coding for Vg in the fat body.

In L. migratoria, Vg synthesis can also be induced (in last stage nymphs and adults) by the ovary maturating parsin (Lom OMP), a neuropeptide from the brain, but ovariectomized nymphs failed to respond, suggesting the participation of a factor from the ovaries, possibly (as in Diptera) 20HE (Girardie & Girardie 1996). Moreover, it has been shown that Lom OMP has two distinct but complementary gonadotropic effects: (i) an ecdysteroidogenic effect triggered by its C-terminal domain with the ovary as the target tissue; and (ii) a protecting effect on Vg mRNA probably provided by its other gonadotropic domain, the N-terminal, with the fat body as the target tissue (Girardie et al. 1998). However, it is clear that JH is the principal hormone in locusts, since in the adult it is the only hormone that regulates the expression of Vg genes.

In the cricket Acheta domesticus (L.), JH controls the transcription of Vg genes and synthesis of Vg polypeptides, which are exported into the hemolymph (Bradley & Edward 1978; Benford & Bradley 1986; Strambi et al. 1997). In Gryllus bimaculatus (De Geer), the time of the first appearance of Vg in the hemolymph coincides with the onset of JH synthesis by the CA (Kempa-Tomm et al. 1989, 1990), suggesting the involvement of JH in Vg synthesis. JH III is the major JH in many gryllid crickets such as A. domesticus, Teleogryllus commodus (Le Guillou) and G. bimaculatus (see Strambi et al. 1997). The allatectomy completely abolished oocyte development in A. domesticus, but it did not totally suppress the ovarian development and egg-laying in T. commodus, G. bimaculatus and Gryllus campestris (L.) (see Strambi et al. 1997) as in Rhodnius prolixus (Stål) (Pratt & Davey 1972; Wang & Davey 1993).

Unlike the stimulatory effect of ecdysteroids on Vg synthesis in Locusta (Girardie et al. 1992, 1996, 1998; Girardie & Girardie 1996) and G. bimaculatus (Behrens & Hoffmann 1983) as in the cockroach Blabarus craniifer Burm. (Perriere et al. 1993), ecdysteroids inhibited Vg synthesis in other insects, notably the cockroaches Diploptera (Friedel et al. 1980) and Leucophaea (Engelmann 1979, 2002). Recently, Hatle et al. (2003) have shown that in the lubber grasshopper Romalea microptera (Houttuyn), ecdysteroids have no effect on Vg synthesis, which is different from other orthopterans. Thus the role of ecdysteroids in reproduction of non-dipteran insects is not yet clearly defined (Gade et al. 1997; Tawfik et al. 1997).

Hemiptera

JH is the principal hormone governing Vg synthesis in Hemiptera. Most of the data available is from R. prolixus (Davey 1993) in which JH is responsible for Vg production in the fat body. Similar data have been reported from other heteropteran species including both haematophagous bugs such as Triatoma protracta (Uhler), and phytophagous ones like O. fasciatus and Pyrrhocoris apterus (L.) (Engelmann 1983). In R. prolixus, the synthesis of Vg is stimulated by a low dose of methoprene (Chinzei et al. 1994). Allatectomy has been shown to halt or severely retard egg development in O. fasciatus, Triatoma infestans (Klug), Dindymus versicolor (Herrich-Schäffer), Dysdercus cigulatus (F.), Dysdercus intermedius (Dist.) and Dysdercus koenigii (F.) (see Davey 1997 and references therein). There appear, however, to be some differences in the requirement for JH for Vg production in R. prolixus and O. fasciatus, where allatectomy did not lead to a complete cessation of egg production (Pratt & Davey 1972; Kelly & Hunt 1982; Wang & Davey 1993). In many hemipteran species, JH not only induces Vg synthesis in the fat body (Coles 1965; Mundall & Engelmann 1977), but also controls the access of the Vg molecule to the oocyte (Davey 1993) and its uptake by the oocytes (Wang & Davey 1992). Also, topical application of JHs or their analogues to diapausing individuals of a variety of Hemipteran terminated the reproductive diapause. Riptortus clavatus females developed vitellogenic oocytes after being treated with Altosid (methoprene) (Numata & Hidaka 1984), JH I or JH II (Shinoda et al. 1996). However, fewer vitellogenic follicles were produced when females were treated with JH III. This is in contrast in the two-spotted stinkbug Perillus bioculatus (F.), where JH III is involved in ovarian maturation and Vg synthesis (Adams et al. 2002).

Recently, we have cloned a Vg gene transcript from the giant water bug L. deyrollei (Nagaba et al. 2010), and demonstrated that Vg gene expression was induced when females in reproductive diapause were injected with JH III and inhibited when they were injected with 20E, suggesting that the Vg gene is regulated by the JH in this species. Also, we have cloned a cDNA encoding Vg showing its differential expression profiling in two wing-morphs of the brown plant-hopper Nilaparvata lugens Stål (Tufail et al. 2010), and reported that the topical application of JH III up-regulated the Vg gene expression, which suggests that the Vg gene is regulated by JH in this species.

Thus, all Hemipteran species examined so far have shown Vg gene regulation by JH. In most cases, the expression of the Vg gene seems to be dependent only on JH, except in R. prolixus and O. fasciatus, where Vg can be expressed apparently in the absence of JH.

Coleoptera

In Coleoptera, the effect of JH on Vg induction has been studied in detail in the Colorado beetle Leptinotarsa decemlineata Say. JH also regulates Vg synthesis in Tenebro molitor L. (Engelmann 1983) and in the lady beetle Coccinella septempunctata L. (Zhai et al. 1984; Zhai & Zhang 1984; Zhang & Zhai 1985). Vg was also induced by a JH analogue in two other lady beetles, Propylea japonica (Thunberg) and Harmonia axyridis (Pallas) (Shen et al. 1992). In some cases, JH treatment alone is insufficient to induce Vg gene transcription. For example, Panaitof and Scott (2006) tried to identify the effect of JH on Vg gene expression in burying beetles Nicrophorus orbicollis (Say) and suggest that JH alone is not sufficient to up-regulate the expression of Vg genes and that other factors may be involved in regulating their vitellogenic cycle as well. Recently, in the red flour beetle Tribolium castaneum (Herbst) it was reported that Vg gene induction requires both JH and 20E (Parthasarathy et al. 2010). However, Vg mRNA was induced by the application of JH III but not by the injection of 20E into previtellogenic females. These data suggest that JH is required for Vg synthesis in the fat body and 20E influences Vg synthesis through its action on oocyte maturation.

Lepidoptera

Hormonal regulation of Vg gene transcription varies in this group as suggested by Belles (1998). Vg transcription is controlled by ecdysteroids in species where vitellogenesis starts in larvae or early pupal stages while both ecdysteroid and JH are required in species where Vg expression starts before adult emergence in the pharate adults. On the other hand, Vg gene expression is regulated solely by JH in species where Vg expression starts after adult emergence. For example in H. cecropia and B. mori Vg synthesis starts in early pupal stages and is regulated by the 20E (Tsuchida et al. 1987). Similar is the case in Lymantria dispar (L.) where vitellogenesis begins in late instar larvae. In L. dispar, the topical application of JH even inhibits Vg gene expression (Fescemyer et al. 1992) suggesting that a declining or low JH titer is crucial for Vg induction in this species. In the fall armyworm Spodoptera frugiperda (Smith), expression of the Vg gene is regulated by both JH and ecdysteroids; however, Vg uptake by developing oocytes seems to be controlled only by JH (Sorge et al. 2000). Instead, Vg gene transcription is controlled only by JH in Heliothis virescens F. (Zeng et al. 1997) and in several other members of Lepidoptera where vitellogenesis starts after adult emergence (Cusson et al. 1994).

Diptera

Diptera reveal an intricate mechanism of reproductive regulation involving multiple hormones. Yin and Stoffolano (1997) suggested that dipterans are too diverse as a group, and even hormonal regulation varies within Cyclorrapha and Nematocera. In Nematocera, typically the mosquito Ae. aegypti (Hagedorn 1985; Raikhel 1992; Dhadialla & Raikhel 1994) the role of 20E on Vg gene expression has been demonstrated. Also, it was shown that JH potentiates the action of 20E by inducing capacitation of the fat body during the previtellogenic phase. In addition, some anautogenous mosquitoes, such as Ae. aegypti and Culex pipiens pipiens (L.) must take a blood meal for activation of Vg genes. In contrast, autogenous mosquitoes like Ae. taeniorhynchus (Wiedemann), Ae. atropaplus (Coquillett), Culex pipiens molestus (Forskål) can produce one set of eggs using nutritional reserves stored during their larval phase, but need a blood meal for subsequent egg formation. However, hormonal regulation of Vg induction appears to be similar in both groups of mosquitoes (Klowden 1997).

In Cyclorrapha, typically D. melanogaster (Meigen), both JH and 20E stimulate the yolk protein expression both in the fat body and ovary in this species (see review by Kelly 1994). Also, Vg induction has been directed both by JH and 20E in the housefly Musca domestica L. (Adams & Filipi 1988). It has been reported that 20E regulate Vg expression both in the ovary and fat body while the effect of JH was greater in the ovary than in the fat body (Agui et al. 1991).

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References

Recent molecular studies have demonstrated that Vg genes encode the major egg yolk protein precursors that belong to a large superfamily of molecules known as large lipid transport proteins (Babin et al. 1999), and their structures appear to be conserved, in certain amino acid residues and motifs, in organisms as diverged as nematodes and vertebrates (Blumenthal & Zucker-Aprison 1987; Spieth et al. 1991; Chen et al. 1997; Sappington et al. 2002; Tufail & Takeda 2008, 2012). This structural conservation in Vg molecules of diversified taxa is, perhaps, because of the same nutritional demands of a developing embryo in all oviparous species. However, great variation has been observed among insects, and even differences exist within the same group, in the number of Vg genes and in the hormonal systems directing these genes. We have proposed that different Vg genes may have different functions (Tufail & Takeda 2008, 2012). The physiological role of Vg other than yolk formation is not ruled out especially when Vg gene expression has been observed in honey bee males (Trenczek & Engels 1986; Valle 1993; Piulachs et al. 2003); also the involvement of the Vg gene in hormonal dynamics in addition to its multiple coordinating effects on social organization in worker bees has been reported (Guidugli et al. 2005; Nelson et al. 2007). Vgs are also reported to have important antioxidant activities and prolong lifespan in honey bee and Caenorhabditis elegans Maupas (Nakamura et al. 1999; Seehuus et al. 2006) and are involved in promoting macrophage phagocytosis in fish (Li et al. 2008). Also, Vg has been reported to reduce the parasite-killing efficiency of the antiparasitic factor thioester-containing protein 1 (TEP1) in Anopheles gambiae Giles (Rono et al. 2010), and has shown anti-bacterial activity in B. mori (Singh et al. 2013), thus suggesting some link of this protein with immunity. Future studies must elucidate the physiological roles of multiple Vg genes in other than reproduction.

The hormonal system regulating Vg transcription varies greatly among various insect groups and differences exist even within the same group and the same family. However, the overall understanding that has emerged is that most insect species investigated use JH to govern the regulation of Vg gene transcription (Engelmann 1983; Wyatt & Davey 1996; Belles 1998; Raikhel et al. 2004; Tufail & Takeda 2012). On the other hand, some insects, such as dipterans (mosquitoes and D. melanogaster), require ecdysone, a product from ovaries (Hagedorn et al. 1975) in addition to JH, while lepidopterans require JH, ecdysteroids and additional hormones to regulate their reproductive biology. However, why insect species diverge in using different hormones to govern their reproductive physiology remains unclear. Also, the molecular mechanism of hormonal regulation of Vg gene transcription, especially for JH, remains an important issue for future research.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Biochemical and molecular aspects of insect vitellogenins
  5. Vg genes and their regulation in insects
  6. Vg gene as a target of endocrine disruptors
  7. Molecular mechanism of Vg gene transcription
  8. Hormonal regulation of Vg gene transcription in different insect groups
  9. Conclusions
  10. Acknowledgments
  11. References
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