chapter 1 - Bentham Science

Hemolymph Proteins and Functional Peptides: Recent Advances in Insects and Other Arthropods Vol. 1, 2012, 111-127 111
Muhammad Tufail and Makio Takeda (Eds)
All rights reserved-© 2012 Bentham Science Publishers
CHAPTER 7
Neurohormones and Second Messengers in Lepidoptera: Male Sexual
Development and Midgut Growth †
Marcia J. Loeb *
U.S. Department of Agriculture, Insect Biocontrol Laboratory, Beltsville, MD 20705, USA
Abstract: The insect brain peptides that induce target tissues to secrete steroid hormones, the ecdysones, are
quite different from each other in peptide sequences and structures. Therefore, it is probable that related
differences in specific receptors for the peptides exist on target organs, allowing for specific patterns of
ecdysteroid synthesis by those tissues coordinated with regulation of metamorphosis. We identified and
characterized an ecdysiotropic peptide from brains of Lymantria dispar that induced sheaths of testes to
secrete ecdysteroid in vitro. The ecdysteroid in turn promoted synthesis of at least one peptide by fat body
and/or testis sheaths that promoted sperm maturation and male gonadal imaginal disc development in vitro.
We have cultured midgut stem cells and identified two peptidic factors controlling stem cell multiplication:
the fast-acting brain peptide Bombyxin and the slower-acting fat body peptide, alpha-arylphorin. It is not
known how these factors enter midgut cells, how they are processed, or how they incite stem cells to divide.
We have characterized 4 differentiation-promoting growth factors, the MDFs, from culture medium and
hydrolyzed hemolymph. They direct differentiation to normal and abnormal midgut cell fates. Internal
[Ca 2+ ] may be a second messenger for MDFs. Antibodies to the MDFs have revealed MDFs 1-4 in
columnar cells and MDF4 in secretory cells as well. MDF2 appeared in the gut lumen, and MDF 4 is
released from midgut secretory cells to both gut lumen and hemolymph.
Keywords: Neurohormones, ecdysteroidogenic peptides, second messengers, brain, role of testes,
spermatogenesis, growth factors, fat body, midgut differentiation factors, Lepidoptera.
1. INTRODUCTION AND ECDYSTEROIDOGENIC PEPTIDES FROM THE BRAINS OF
INSECTS
Insect growth and development occur at each genetically destined molt. Every molt is a complicated
process that depends on discrete changes in gene expression, hormonal secretory activity [1-2] mitotic
activity and creation of new cell types and tissues, cell death and behavior [3]. A molt is generally induced
by release of a large (14-29 KDa) peptide hormone, prothoracicotropic hormone (PTTH) from the brain
that activates its target organs, the prothoracic glands, to synthesize and release a steroid hormone (or a
complex of similar steroid hormones, the ecdysteroids). This rise in ecdysteroid hormone titer in the
hemolymph is correlated with a drop in the titer of one or more of the long chain terpenoid juvenile
hormones secreted by the corpora allata or ring glands [1, 2, 4, 5]. Several brain and terminal abdominal
ganglion peptides, some previously identified as myosuppressins, FMRFamides and allatostatin B, are
actually prothoracicostatic peptides3 (PTSPs) that have been isolated from the lepidopteran, Bombyx mori.
They inhibit PTTH secretion and lead to a decline in ecdysteroid synthesis just before the actual molt [6].
The corpora allata are directly controlled by other brain peptides, various biochemical versions of
allatotropins and allatohibins [4, 7, 8]. A small PTTH, (3-7 KDa), an insulin-like peptide, has been isolated
from B. mori brains. It also induces ecdysteroid production by prothoracic glands in some insects, but has
other physiological functions as well, and is now known as Bombyxin [9-12]. Other brain peptides control
ecdysteroid synthesis by other organs. The ecdysiotropic hormone, Egg Development Neurohormone
(EDNH) (also known as Ovarian Ecdysteroidogenic Hormone, or OEH), induces insect ovaries to
synthesize ecdysteroid [13]. Ovarian ecdysteroids modulate fat body secretion of yolk proteins that are
stored in the oocyte, and there support embryonic development as well as synthesis of the vitelline
*Address correspondence to Marcia J. Loeb: 6920 Fairfax Rd. Bethesda MD 20814, USA; Phone: +1 301-652-4229; Email:
geo.mar2@verizon.net
† This article is a US government work, and, as such, is in the public domain in the United States of America.