Developmental Expression Pattern of
Monoamine Oxidases in Sensory Organs
and Neural Crest Derivatives
TANIA VITALIS,
1
CHANTAL ALVAREZ,
2
KEVIN CHEN,
3
JEAN C. SHIH,
3
PATRICIA GASPAR,
2
AND OLIVIER CASES
2
*
1
Department of Anatomy and Developmental Biology, University College London,
WC1E6BT London, United Kingdom
2
Institut National de la Sante ´ et de la Recherche Me ´dicale U106, Ba ˆ timent de Pe ´diatrie,
Ho ˆpital de la Pitie ´-Salpe ˆtrie `re, 75013 Paris, France
3
Department of Pharmacology and Toxicology, Pharmaceutical Science Center,
University of Southern California, Los Angeles, California 90033
ABSTRACT
Serotonin (5-HT) has been shown to act as a morphogen in craniofacial and heart
development and in the migration of neural crest derivatives. Some of these structures are
capable of capturing 5-HT during development, but nothing is known about the localization
of the main monoamine degradation enzymes, monoamine oxidase (MAO) A and B, in these
developing tissues. We generated a highly specific antibody to MAOB; immunoreactivity is
entirely abolished in brain extracts or brain sections of mice lacking MAOB. From the use of
this antibody and specific riboprobes, we report that MAOB is expressed early in a variety of
neural crest derivatives, in facial sensory organs, and in the heart. From E11.5 to P0, MAOB
was found to be strongly expressed in the following neural crest derivatives: the aorta, cranial
mesenchyme (developing bones, sensory neurons of the cranial ganglia, cartilages, thyroid,
and striate muscles), dental mesenchyme, several soft palate derivatives, and boundary cap
cells (E11.5–P4). Boundary cap cells contribute to the formation of nerve exit– entry points
between the central and the peripheral nervous systems. Several facial sensory organs also
contained MAOB mRNA, protein, and activity. High MAOB expression was noted in the
olfactory placode, the dorsal part of the olfactory epithelium, the olfactory nerve layer
(probably the ensheathing glia), the cochlear ganglionic cells, the taste buds, and the Merkel
cells in the vibrissae follicles. Finally, we found that MAOB is massively expressed in the
pharyngeal organ, heart, liver, and mast cells. In contrast, MAOA expresssion was restricted
to the sympathetic ganglia and to the meningeal and capillary blood vessels. The pattern of
MAOB expression generally matched the previously reported patterns of expression of the
plasma 5-HT transporter expression or of the histamine biosynthetic enzyme L-histidine
decarboxylase, suggesting a role for MAOB in fine regulation of the levels of 5-HT and
histamine in the developing embryo. J. Comp. Neurol. 464:392– 403, 2003.
© 2003 Wiley-Liss, Inc.
Indexing terms: serotonin; histamine; plasma serotonin transporter; vesicular monoamine
transporter; olfactory epithelium; cranial neural crest
Grant sponsor: Institut National de la Sante ´ et de la Recherche Me ´di-
cale; Grant sponsor: Wellcome Trust; Grant sponsor: National Institute of
Mental Health; Grant number: R37 MH39085; Grant number: R01
MH37020; Grant sponsor: Boyd and Elsie Welin Professorship award
(J.C.S.).
*Correspondence to: Olivier Cases, INSERM U106, Ba ˆ timent de Pe ´dia-
trie, Ho ˆpital de la Pitie ´-Salpe ˆtrie `re, 47 boulevard de l’ho ˆpital, 75651 Paris
Cedex 13, France. E-mail: olicases@infobiogen.fr
Received 7 January 2003; Revised 24 March 2003; Accepted 24 April
2003
DOI 10.1002/cne.10804
Published online the week of August 4, 2003 in Wiley InterScience
(www.interscience.wiley.com).
THE JOURNAL OF COMPARATIVE NEUROLOGY 464:392– 403 (2003)
© 2003 WILEY-LISS, INC.