REPRODUCTION
© 2017 Society for Reproduction and Fertility DOI: 10.1530/REP-16-0377
ISSN 1470–1626 (paper) 1741–7899 (online) Online version via www.reproduction-online.org
RESEARCH
Gonadotropin characterization, localization and expression in
the European hake (Merluccius merluccius)
Michela Candelma
1
, Romain Fontaine
2
, Sabrina Colella
3
, Alberto Santojanni
3
,
Finn-Arne Weltzien
2
and Oliana Carnevali
1
1
Department of Life and Environmental Sciences, Università Politecnica delle Marche, Ancona, Italy,
2
Department of
Basic Sciences and Aquatic Medicine, Norwegian University of Life Sciences, Oslo, Norway, and
3
CNR-National
Research Council of Italy, ISMAR-Marine Sciences Institute, Ancona, Italy
Correspondence should be addressed to O Carnevali; Email: o.carnevali@univpm.it
Abstract
In vertebrates, the regulation of gametogenesis is under the control of gonadotropins (Gth), follicle-stimulating hormone (Fsh) and
luteinizing hormone (Lh). In fsh, the physiological role of Gths is not fully understood, especially in species with asynchronous
ovarian development. To elucidate the role of Gths in species with asynchronous ovary, we studied European hake (Merluccius
merluccius) during the reproductive season. For this aim, we frst cloned and sequenced both hormones. Then, we characterized their
amino acid sequence and performed phylogenetic analyses to verify the relationship to their orthologues in other species. In addition,
the quantifcation of gene expression during their natural reproductive season was analyzed in wild-caught female hake. Our results
revealed that fshb peaked during the vitellogenic phase, remaining high until spawning. This is in contrast to the situation in species
with synchronous ovary. lhb, on the other hand, peaked during maturation as it is also common in species with synchronous ovarian
development. Finally, combining double-labeling fuorescent in situ hybridization (FISH) for Gth mRNAs with immunofuorescence
for Lh protein, we evidenced the specifc expression of fshb and lhb in different cells within the proximal pars distalis (PPD) of the
pituitary. In addition to gonadotrope cells specifc to expression of either fshb or lhb, some cells showed co-expression of both genes.
This suggests either that gonadotropes with co-expression are not yet specifed or they could have a plasticity that permits changes
from one cell phenotype to another during certain life stages and in turn during different physiological states.
Reproduction (2017) 153 123–132
Introduction
The pituitary gonadotropins, follicle-stimulating hormone
(Fsh) and luteinizing hormone (Lh) are hormones directly
involved in regulation of gametogenesis in vertebrates
(Nagahama 1994, Swanson et al. 2003, Weltzien
et al. 2004). Both gonadotropins are heterodimeric
glycoproteins and consist of a common α subunit shared
with thyroid-stimulating hormone (Tsh) and a hormone-
specifc β subunit important for their biological specifcity.
Fsh and Lh are secreted by gonadotropes present
mainly in proximal pars distalis (PPD) and some cells
of pars intermedia (PI) of the pituitary gland in teleosts
(Weltzien et al. 2003a). In mammals, the gonadotrope
cells produce both gonadotropins (Nakane 1970)
and rarely an overlapped expression was found. On
the contrary, in teleosts, Fsh and Lh are synthesized
by two different cell types (Zohar et al. 2010) and
the colocalization of the two mRNAs in the same
gonadotrope cell was only occasionally evidenced
(García Hernández et al. 2002, Weltzien et al. 2014).
Because of the variety of reproductive strategies in
different teleost species, the physiological roles of the two
gonadotropins during the ovarian cycle do not seem to
be the same for all species. Following Tyler and Sumpter
(1996), reproductive strategies can be differentiated on the
basis of the dynamics of ovarian development: ovaries can
be classifed as synchronous or asynchronous, even though
such division could be reductive due to the wide number
of reproductive strategies. The species with synchronous
ovaries spawn eggs once within the reproductive season.
These species are characterized by increasing plasma
levels of Fsh with ovarian development (Tyler et al. 1997),
whereas Lh surges during fnal maturation and spawning
(Planas & Swanson 1995, Gomez et al. 1999, Yoshiura
et al. 1999, Schmitz et al. 2005).
The regulatory mechanism of gonadotropins during
gametogenesis is not so clear when we consider the
teleosts with asynchronous ovaries, i.e., the species that
spawn multiple batches of oocytes during the reproductive
season. For instance in chub mackerel (Scomber
japonicus), fshb mRNA levels increase during the frst
stages of ovarian cycle, peaking at the end of vitellogenesis,
whereas lhb mRNA levels signifcantly increase during late
vitellogenesis. Finally, the mRNA levels for both hormones
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