Characterization of CXC-type chemokine molecules
in early Xenopus laevis development
TOSHIYASU GOTO
1
, TATSUO MICHIUE
2
, YUZURU ITO
3
and MAKOTO ASASHIMA*
,2,3
1
Department of Molecular Cell Biology, Medical Research Institute and School of Biomedical Science, Tokyo Medical
and Dental University, Tokyo,
2
Department of Life Sciences (Biology), Graduate School of Arts and Sciences, The
University of Tokyo, Tokyo and
3
Research Center for Stem Cell Engineering, National Institute of Advanced Industrial
Science and Technology (AIST), Tsukuba, Japan
ABSTRACT Chemokine molecules play important roles in the immune system. However, several
chemokine molecules are expressed during early development before the immune system is es-
tablished. Using reverse transcription–polymerase chain reaction (RT-PCR) and overexpression of
chemokine molecules, we identified and characterized Xenopus laevis CXC-type chemokine ligands
(XCXCL13L1, XCXCL13L2, XCXCLa, XCXCLb, XCXCLd, and XCXCLe) and receptors (XCXCR1/2,
XCXCR3, XCXCR5, XCXCR6, and XCXCRa) during early development. The CXC-type ligands have
low identity with genes for human CXC ligands (CXCL). With the exception of XCXCRa, the CXC
receptors (CXCR) identified in the present study had high (~40%–65%) identity with human CXCR
genes. Although the expression patterns for the CXCL and CXCR genes differed, transcript levels for
all genes were very low during early embryogenesis. Overexpression of XCXCL13L1, XCXCL13L2,
XCXCLa, XCXCR3, XCXCR6, and XCXCRa interfered with gastrulation and neural fold closure. The
results of the present study suggest that several chemokine molecules are related to cell move-
ments during early morphogenesis.
KEY WORDS: chemokine, CXC receptor, CXC ligand, gastrulation, Xenopus laevis
Introduction
Chemokine ligands are considered cytokine molecules and,
in mammals, have been investigated primarily in terms of their
immunomodulatory role. Mammalian chemokines are divided into
four families, namely CC-, CXC-, XC-, and CX3C-type chemokines,
which contain 28, 17, 2, and 1 member, respectively (Laing and
Secombes, 2004; Hiraoka et al., 2011). Chemokine receptors are
members of the G-protein-coupled receptor (GPCR) family and
have seven transmembrane structures. The chemokine receptors
are also divided into four families according to ligand type: CC-,
CXC-, XC-, and CX3C-type receptors, containing 10, 7, 1, and 1
member, respectively (Allen et al., 2007).
Seventeen CXC-type chemokines have been identifed and
characterized in mammals (Laing and Secombes, 2004). The
CXC chemokines are further divided into two groups depending
on the presence (+) or absence (–) of the tripeptide motif glutamic
acid–leucine–arginine (ELR) at the N-terminus of the frst cysteine
residue. The CXC ligands (CXCL) CXCL1, CXCL2, CXCL3, CXCL5,
CXCL6, CXCL7, CXCL8, and CXCL15 belong to the ELR(+) group
Int. J. Dev. Biol. 57: 41-47 (2013)
doi: 10.1387/ijdb.120223ma
www.intjdevbiol.com
*Address correspondence to: Makoto Asashima. Department of Life Sciences (Biology), Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1
Komaba, Meguro-ku, Tokyo 153-8902, Japan. Tel: +81-3-5454-6632. Fax: +81-3-5454-6698. e-mail: asashi@bio.c.u-tokyo.ac.jp
Accepted: 7 November 2012. Final, author-corrected PDF published online: 8th March 2013. Edited by: Makoto Asashima.
ISSN: Online 1696-3547, Print 0214-6282
© 2013 UBC Press
Printed in Spain
Abbreviations used in this paper: CXCL, CXC ligand; CXCR, CXC receptor; PGC,
primordial germ cell; RT-PCR, reverse transcription-polymerase chain reaction.
(Romagnani et al., 2004; Wang et al., 2005). It has been reported
that CXCL1–CXCL8 bind to the CXC receptor (CXCR) CXCR2,
but a receptor for CXCL15 is yet to be unidentifed (Zlotnik and
Yoshie, 2000; Wang et al., 2005). Specifcally, CXCR1 binds CXCL1,
CXCL6, and CXCL8 (Zlotnik and Yoshie, 2000); CXCR3 and its
alternatively splicing variant bind CXCL4, CXCL9, CXCL10, and
CXCL11 (Zlotnik and Yoshie, 2000; Lasagni et al., 2003); CXCR4
binds CXCL12; CXCR5 binds CXCL13; CXCR6 binds CXCL16;
and, CXCR7 binds CXCL11 and CXCL12 (Zlotnik and Yoshie,
2000; Naumann et al., 2010; Agostini et al., 2005). No receptors
have been identifed as yet for CXCL14 and CXCL17 (Hara and
Tanegashima, 2012; Hiraoka et al., 2011).
Recent studies have revealed that several chemokine ligands
and receptors have important roles in early embryogenesis in
vertebrates before the immune system is established. For ex-
ample, CXCL12/CXCR4 promotes directional movement of pri-
mordial germ cell (PGC) migration in zebrafsh (Doitsidou et al.,