Insect Biochem. Vol. 15, No. 6, pp. 735-747, 1985 0020-1790/85 $3.00+ 0.00
Printed in Great Britain. All rights reserved Copyright © 1985Pergamon Press Ltd
BINDING OF VITELLOGENIN TO SPECIFIC RECEPTORS
IN OOCYTE MEMBRANE PREPARATIONS OF THE
OVOVIVIPAROUS COCKROACH NAUPHOETA CINEREA
ROLF KONIG and BEATRICELANZREIN
Division of Animal Physiology, University of Berne, Erlachstrasse 9a, CH-3012 Berne, Switzerland
(Received 15 November 1984; revised and accepted 15 May 1985)
Abstract--An in vitro binding assay was developed to investigate the presence of specific binding sites for
vitellogenin in oocyte membrane preparations of a cockroach. Vitellogenin binding reached equilibrium
within 1 hr at both 4 and 26°C and was shown to be pH-dependent, specific, saturable and tissue specific.
Analysis of saturation isotherms revealed a concentration of receptors of 120 fmol per oocyte near the
middle of the first vitellogenic cycle. The amount of vitellogenin bound per oocyte increased progressively
during oocyte maturation. Scatchard analysis revealed a K a of 5 x 10 -7 M, and determination of the rate
constants for association and dissociation yielded a similar Kd-value. Oocyte membrane preparations of
Nauphoeta cinerea did not bind vitellogenin of the closely related cockroach, Leucophaea maderae, whereas
oocyte membranes of the latter species did bind the vitellogenin of Nauphoeta cinerea.
Key Word Index: Cockroach, vitellogenin, oocytes, specific binding, receptor-mediated endocytosis,
kinetic analysis
INTRODUCTION
Vitellogenins are the predominant yolk protein pre-
cursors in egg-laying animals. Their synthesis is hor-
monally controlled and takes place in the vertebrate
liver and the insect fat body. Vitellogenins are se-
creted into the blood and sequestered by the maturing
oocytes against a concentration gradient (for reviews
see Wallace, 1978; Engelmann, 1979, 1983; Hagedorn
and Kunkel, 1979). In most insect species the sesqui-
terpenoid juvenile hormone induces vitellogenin syn-
thesis, and indirect evidence suggests that the uptake
of vitellogenin is also influenced by juvenile hormone
(Bell and Barth, 1971; Wilhelm and Liischer, 1974;
Sams and Bell, 1977; Giorgi, 1979; Postlethwait and
Handler, 1979; Davey, 1981).
Animal cells sequester nutritional and regulatory
proteins from extracellular fluids by receptor-
mediated endocytosis. According to a model devel-
oped for the uptake of low density lipoprotein by
human fibroblasts, this process involves the binding
of the protein molecules to membrane-associated
receptors and the internalization of the
receptor-ligand complexes by micropinoeytosis
(Brown and Goldstein, 1979). A similar mechanism is
proposed for the incorporation of immunoglobulins
and yolk proteins by chicken oocytes (Roth et aL,
1976; Yusko and Roth, 1976), asialoglycoproteins by
hepatocytes (Kolb-Bachofen, 1981), yolk proteins by
oocytes of Xenopus (Opresko et aL, 1980) and Aedes
aegypti (Roth and Porter, 1964; Roth et al., 1976), as
well as for the uptake of several protein hormones by
their respective target tissues (for reviews see Gold-
stein et aL, 1979; Kaplan, 1981). The presence of
coated pits and coated vesicles has been demon-
strated in Aedes aegypti using electron microscopy
(Roth and Porter, 1964) and chicken oocyte mem-
branes have been shown to bind vitellogenin
specifically (Yusko and Roth, 1976). To study the
role of juvenile hormone in the regulation of the
uptake of vitellogenin, the mechanism of vitellogenin
recognition and incorporation has first to be eluci-
dated. The oocyte structure in our experimental
insect, the ovoviviparous cockroach, Nauphoeta
cinerea, has been studied in detail (W/Jest, 1979) and
the endocrine control of oocyte maturation (Wilhelm
and L/Jscher, 1974; B/jhlmann, 1976; Lanzrein et al.,
1978), and the competence of oocytes to incorporate
vitellogenin (Buschor et al., 1984) have been in-
vestigated. Furthermore, vitellogenin and vitellin
have been isolated (Buschor and Lanzrein, 1983) and
characterized (Imboden et al., 1986) in this species. In
the present paper we describe a vitellogenin binding
assay and show vitellogenin binding to oocyte mem-
brane preparations to be specific, saturable and tissue
specific. The kinetic and equilibrium properties of
vitellogenin binding to membrane preparations of
maturing oocytes are characterized. In addition we
demonstrate that oocyte membrane preparations of
Nauphoeta cinerea do not bind vitellogenin of the
related species Leucophaea maderae, whereas oocyte
membrane preparations of the latter bind vitellogenin
of the former.
MATERIALSAND METHODS
Insects
Nauphoeta cinerea and Leucophaea maderae were kept at
26°C and 60% r.h. on dog flakes and water at a photoperiod
of 12 hr. Under these conditions, oocyte maturation in N.
cinerea was 12-13 days and in L. maderae 22-26 days.
Gestation was 40-42 days in the former and approx. 60 days
in the latter.
Chemicals
All chemicals were of analytical grade and were pur-
chased from Merck and Co. if not otherwise stated. Sub-
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