Oocyte membrane localization of vitellogenin receptor coincides with queen flying age, and receptor silencing by RNAi disrupts egg formation in fire ant virgin queens

FEBS Journal

Volumn 276, Issue 11, 2009, Pages 3110-3123

  Lu, Hsiao Ling ^a   Vinson, S B ^a   Pietrantonio, Patricia V ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Insect ovary; Insect reproduction; Oocyte development; RNA interference; Social insects

Indexed keywords

VITELLOGENIN;

ANT; ARTICLE; CONTROLLED STUDY; EGG PRODUCTION; FEMALE; IMMUNOFLUORESCENCE TEST; MALE; MATING SYSTEM; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUEEN (INSECT); RNA INTERFERENCE;

ANIMALS; ANTS; BLOTTING, WESTERN; CELL MEMBRANE; EGG PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MALE; MEMBRANE PROTEINS; OOCYTES; OVARY; OVUM; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TIME FACTORS;

FORMICIDAE; HEXAPODA; HYMENOPTERA; SOLENOPSIS GEMINATA; SOLENOPSIS INVICTA;

EID: 65549127222     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07029.x     Document Type: Article

References (72)

1. Wilson EO (1971) The Insect Societies. Harvard University Press, Cambridge, MA.
2. Sappington TW Raikhel AS (1998) Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem Mol Biol 28, 277 300. (Pubitemid 28328322)
3. Sappington TW Raikhel AS (2004) Insect vitellogenin/yolk protein receptors. In Progress in Vitellogenesis, Reproductive Biology of Invertebrates, Vol. 7, Part B (Raikhel AS Sappington TW eds pp. 229 264. Science Publishers, Enfield, NH.
4. Snigirevskaya ES Raikhel AS (2004) Receptor mediated endocytosis in insect oocytes. In Progress in Vitellogenesis. Reproductive Biology of Invertebrates, Vol. 7 (Raikhel AS Sappington TW eds pp. 199 228. Science Publishers, Enfield, NH. (Pubitemid 38496510)
5. Raikhel AS, Brown MR Belles X (2005) Hormonal control of reproductive processes. In Comprehensive Molecular Insect Science, Vol. 3 (Gilbert LI, Iatrou K Gill SS eds pp. 433 491. Elsevier, Amsterdam.
6. Swevers L, Raikhel AS, Sappington TW, Shirk P Iatrou K (2005) Vitellogenesis and post-vitellogenic maturation of the insect ovarian follicle. In Comprehensive Molecular Insect Science, Vol. 3 (Gilbert LI, Iatrou K Gill SS eds pp. 87 155. Elsevier, Amsterdam.
7. Schonbaum CP, Lee S Mahowald AP (1995) The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proc Natl Acad Sci USA 92, 1485 1489.
8. Sappington TW, Kokoza VA, Cho WL Raikhel AS (1996) Molecular characterization of the mosquito vitellogenin receptor reveals unexpected high homology to the Drosophila yolk protein receptor. Proc Natl Acad Sci USA 93, 8934 8939. (Pubitemid 26281995)
9. Ciudad L, Piulachs MD Belles X (2006) Systemic RNAi of the cockroach vitellogenin receptor results in a phenotype similar to that of the Drosophila yolkless mutant. FEBS J 273, 325 335.
10. Tufail M Takeda M (2005) Molecular cloning, characterization and regulation of the cockroach vitellogenin receptor during oogenesis. Insect Mol Biol 14, 389 401. (Pubitemid 41577058)
11. Tufail M Takeda M (2007) Molecular cloning and developmental expression pattern of the vitellogenin receptor from the cockroach, Leucophaea maderae. Insect Biochem Mol Biol 37, 235 245. (Pubitemid 46216815)
12. Guidugli-Lazzarini KR, Nascimento AM, Tanaka ED, Piulachs MD, Hartfelder K, Bitondi MG Simoes ZLP (2008) Expression analysis of putative vitellogenin and lipophorin receptors in honey bee (Apis mellifera L.) queens and workers. J Insect Physiol 54, 1138 1147.
13. Guidugli KR, Nascimento AM, Amdam GV, Barchuk AR, Omholt S, Simoes ZL Hartfelder K (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett 579, 4961 4965. (Pubitemid 41242836)
14. Bloch G, Sullivan JP Robinson GE (2002) Juvenile hormone and circadian locomotor activity in the honey bee Apis mellifera. J Insect Physiol 48, 1123 1131. (Pubitemid 35426625)
15. Hartfelder K, Bitondi MM, Santana WC Simoes ZL (2002) Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? Insect Biochem Mol Biol 32, 211 216. (Pubitemid 34076085)
16. Hartfelder K Emlen DJ (2005) Endocrine control of insect polyphenism. In Comprehensive Molecular Insect Science, Vol. 3 (Gilbert LI, Iatrou K Gill SS eds pp. 651 703. Elsevier, Amsterdam.
17. Robinson GE Vargo EL (1997) Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol 35, 559 583. (Pubitemid 127705854)
18. Holldobler B Wilson EO (1990) The Ants. Belknap/Harvard University Press, Cambridge, MA.
19. Wilson EO Holldobler B (2005) The rise of the ants: a phylogenetic and ecological explanation. Proc Natl Acad Sci USA 102, 7411 7414. (Pubitemid 40740986)
20. Vinson SB, Pietrantonio PV, Lu HL Coates CJ (2008) The physiology of reproduction in the imported fire ant, Solenopsis invicta Buren. In Recent Advances in Insect Physiology, Toxicology and Molecular Biology (Liu N ed pp. 153 171. Research Signpost, Kerala, India.
21. Barker JF (1979) Endocrine basis of wing casting and flight muscle histolysis in the fire ant Solenopsis invicta. Experientia 35, 552 554. (Pubitemid 9169207)
22. Davis WL, Jones RG Farmer GR (1989) Insect hemolymph factor promotes muscle histolysis in Solenopsis. Anat Rec 224, 473 478. (Pubitemid 19206364)
23. Tian H, Vinson SB Coates CJ (2004) Differential gene expression between alate and de-alate queens in the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Insect Biochem Mol Biol 34, 937 949. (Pubitemid 40047471)
24. Burns SN, Vander Meer RK Teal PEA (2005) The effect of age and social environment on de-alation in Solenopsis invicta (Hymenoptera: Formicidae) female alates. Fla Entomol 88, 452 457. (Pubitemid 43181427)
25. Keller L Ross KG (1993) Phenotypic plasticity and 'cultural transmission' of alternative social organizations in the fire ant Solenopsis invicta. Behav Ecol Sociobiol 33, 121 129. (Pubitemid 24411766)
26. Tschinkel WR (2008) The Fire Ants. Belknap/Harvard University Press, Cambridge, MA.
27. Harshman LG Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22, 80 86. (Pubitemid 46123724)
28. Voss SH Blum MS (1987) Trophic and embryonated egg production in founding colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Sociobiology 13, 271 278.
29. Fletcher DJ Blum MS (1981) Pheromonal control of de-alation and oogenesis in virgin queen fire ants. Science 212, 73 75. (Pubitemid 11114685)
30. Barker JF (1978) Neuroendocrine regulation of oocyte maturation in the imported fire ant Solenopsis invicta. Gen Comp Endocrinol 35, 234 237. (Pubitemid 9007055)
31. Burns SN, Teal PE, Vander Meer RK, Nation JL Vogt JT (2002) Identification and action of juvenile hormone III from sexually mature alate females of the red imported fire ant, Solenopsis invicta. J Insect Physiol 48, 357 365. (Pubitemid 34492192)
32. LeConte Y Hefetz A (2008) Primer pheromones in social Hymenoptera. Annu Rev Entomol 53, 523 542.
33. Vargo EL Laurel M (1994) Studies on the mode of action of a queen primer pheromone of the fire ant Solenopsis invicta. J Insect Physiol 40, 601 610. (Pubitemid 2107261)
34. Vargo EL (1998) Primer pheromones in ants. In Pheromone Communication in Social Insects: Ants, Wasps, Bees, and Termites (Vander Meer RK, Breed MD, Winston ML Espelie KE eds pp. 293 313. Westview Press, Boulder, CO.
35. Kearney GP, Toom PM Blomquist GL (1977) Induction of de-alation in virgin female Solenopsis invicta with juvenile hormones. Ann Entomol Soc Am 70, 699 701. (Pubitemid 8184885)
36. 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. (Pubitemid 38522250)
37. Brent CS Vargo EL (2003) Changes in juvenile hormone biosynthetic rate and whole body content in maturing virgin queens of Solenopsis invicta. J Insect Physiol 49, 967 974. (Pubitemid 37261722)
38. Toth AL Robinson GE (2007) Evo-devo and the evolution of social behavior. Trends Genet 23, 334 341. (Pubitemid 46962801)
39. Smith CR, Toth AL, Suarez AV Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9, 735 748.
40. Sappington TW, Hays AR Raikhel AS (1995) Mosquito vitellogenin receptor: purification, developmental and biochemical characterization. Insect Biochem Mol Biol 25, 807 817.
41. Amdam GV, Norberg K, Hagen A Omholt SW (2003) Social exploitation of vitellogenin. Proc Natl Acad Sci USA 100, 1799 1802. (Pubitemid 36254528)
42. Seehuus S-C, Norbert K, Krekling T, Fondrk K Amdam GV (2007) Immunogold localization of vitellogenin in the ovaries, hypopharyngeal glands and head fat bodies of honey bee workers, Apis mellifera. J Insect Sci 7, 52, http://www.insectscience.org/7.52/. (Pubitemid 350014239)
43. Obin MS Vander Meer RK (1994) Alate semiochemicals release worker behavior during fire ant nuptial flights. J Entomol Sci 29, 143 151. (Pubitemid 2073073)
44. Alonso AE Vander Meer RK (1997) Source of alate excitant pheromones in the red imported fire ant Solenopsis invicta (Hymenoptera: Formicidae). J Insect Behav 10, 541 555. (Pubitemid 27434108)
45. Schonbaum CP, Perrino JJ Mahowald AP (2000) Regulation of the vitellogenin receptor during Drosophila melanogaster oogenesis. Mol Biol Cell 11, 511 521. (Pubitemid 30112161)
46. Culi J Mann RS (2003) Boca, an endoplasmic reticulum protein required for wingless signaling and trafficking of LDL receptor family members in Drosophila. Cell 112, 343 354. (Pubitemid 36187420)
47. Wilhelm JE, Buszczak M Sayles S (2005) Efficient protein trafficking requires trailer hitch, a component of a ribonucleoprotein complex localized to the ER in Drosophila. Dev Cell 9, 675 685. (Pubitemid 41555149)
48. Sommer B, Oprins A, Rabouille C Munro S (2005) The exocyst component Sec5 is present on endocytic vesicles in the oocyte of Drosophila melanogaster. J Cell Biol 169, 953 963. (Pubitemid 41002871)
49. Lewis DK, Campbell JQ, Sowa SM, Chen M, Vinson SB Keeley LL (2001) Characterization of vitellogenin in the red imported fire ant, Solenopsis invicta (Hymenoptera: Apocrita: Formicidae). J Insect Physiol 47, 543 551. (Pubitemid 32298651)
50. Glancey BM, Stringer CE Bishop PM (1973) Trophic egg production in the imported fire ant, Solenopsis invicta. J Georgia Entomol Soc 8, 217 220.
51. Azizi T, Johnston JS Vinson SB (2008) Initiation of flight muscle apoptosis and wing casting in the red imported fire ant, Solenopsis invicta. Physiol Entomol 34, 79 85.
52. Kubli E (2003) Sex-peptides: seminal peptides of the Drosophila male. Cell Mol Life Sci 60, 1689 1704. (Pubitemid 37041365)
53. Yapici N, Kim YJ, Ribeiro C Dickson BJ (2008) A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451, 33 37.
54. Goodman WG Granger NA (2005) The juvenile hormones. In Comprehensive Molecular Insect Science, Vol. 3 (Gilbert LI, Iatrou K Gill SS eds pp. 320 385. Elsevier, Amsterdam.
55. Zhu J, Chen L Raikhel AS (2003) Posttranscriptional control of the competence factor betaFTZ-F1 by juvenile hormone in the mosquito Aedes aegypti. Proc Natl Acad Sci USA 100, 13338 13343. (Pubitemid 37444743)
56. Tu MP, Yin CM Tatar M (2005) Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. Gen Comp Endocrinol 142, 347 356. (Pubitemid 40780096)
57. Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML, Zhou Y, Partridge L Harshman LG (2005) Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J Insect Physiol 51, 455 464. (Pubitemid 40678868)
58. Boulay R, Hooper-Bui LM Woodring J (2001) Oviposition and oogenesis in virgin fire ant females Solenopsis invicta are associated with a high level of dopamine in the brain. Physiol Entomol 26, 294 299. (Pubitemid 34029861)
59. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci USA 104, 7128 7133. (Pubitemid 47186020)
60. Ament SA, Corona M, Pollock HS Robinson GE (2008) Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc Natl Acad Sci USA 105, 4226 4231.
61. Chen ME Pietrantonio PV (2006) The short neuropeptide F-like receptor from the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Arch Insect Biochem Physiol 61, 195 208.
62. Cerstiaens A, Benfekih L, Zouiten H, Verhaert P, De LA Schoofs L (1999) Led-NPF-1 stimulates ovarian development in locusts. Peptides 20, 39 44. (Pubitemid 29158793)
63. Schoofs L, Clynen E, Cerstiaens A, Baggerman G, Wei Z, Vercammen T, Nachman R, De LA Tanaka S (2001) Newly discovered functions for some myotropic neuropeptides in locusts. Peptides 22, 219 227. (Pubitemid 32155934)
64. Lee KS, You KH, Choo JK, Han YM Yu K (2004) Drosophila short neuropeptide F regulates food intake and body size. J Biol Chem 279, 50781 50789. (Pubitemid 40017816)
65. Lee KS, Kwon OY, Lee JH, Kwon K, Min KJ, Jung SA, Kim AK, You KH, Tatar M Yu K (2008) Drosophila short neuropeptide F signaling regulates growth by ERK-mediated insulin signaling. Nat Cell Biol 10, 468 475.
66. Lynch JA Desplan C (2006) A method for parental RNA interference in the wasp Nasonia vitripennis. Nat Protoc 1, 486 494.
67. Mitchell RD III., Ross E, Osgood C, Sonenshine DE, Donohue KV, Khalil SM, Thompson DM Michael RR (2007) Molecular characterization, tissue-specific expression and RNAi knockdown of the first vitellogenin receptor from a tick. Insect Biochem Mol Biol 37, 375 388. (Pubitemid 46401393)
68. Tiu SH, Benzie J Chan SM (2008) From hepatopancreas to ovary: molecular characterization of a shrimp vitellogenin receptor involved in the processing of vitellogenin. Biol Reprod 79, 66 74.
69. Boldbaatar D, Battsetseg B, Matsuo T, Hatta T, Umemiya-Shirafuji R, Xuan X Fujisaki K (2008) Tick vitellogenin receptor reveals critical role in oocyte development and transovarial transmission of Babesia parasite. Biochem Cell Biol 86, 331 344.
70. DiMario PJ Mahowald AP (1987) Female sterile (1) yolkless: a recessive female sterile mutation in Drosophila melanogaster with depressed numbers of coated pits and coated vesicles within the developing oocytes. J Cell Biol 105, 199 206.
71. Schneider WJ (1996) Vitellogenin receptors: oocyte-specific members of the low-density lipoprotein receptor supergene family. Int Rev Cytol 166, 103 137. (Pubitemid 26118471)
72. Saksena S, Shao Y, Braunagel SC, Summers MD Johnson AE (2004) Cotranslational integration and initial sorting at the endoplasmic reticulum translocon of proteins destined for the inner nuclear membrane. Proc Natl Acad Sci USA 101, 12537 12542. (Pubitemid 39122059)