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Volume 272, Number 4, Issue of January 24, 1997 pp. 2437-2445
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.

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Identification, Sequence, and Expression of an Invertebrate Caveolin Gene Family from the Nematode Caenorhabditis elegans
IMPLICATIONS FOR THE MOLECULAR EVOLUTION OF MAMMALIAN CAVEOLIN GENES

(Received for publication, August 20, 1996, and in revised form, October 23, 1996)

ZhaoLan Tang , Takashi Okamoto ^§ , Pratumtip Boontrakulpoontawee ^¶ , Toshiaki Katada , Anthony J. Otsuka ^¶ and Michael P. Lisanti

From  The Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02142-1479, ^§ Shriners Hospitals for Crippled Children, Massachusetts General Hospital, Department of Anesthesia, Harvard Medical School, Boston, Massachusetts 02114, the ^¶ Department of Biological Sciences, Illinois State University, Normal, Illinois 61790, and the  Department of Physiological Chemistry, Faculty of Pharmaceutical Sciences, Tokyo University, Hongo, Bunkyo, Tokyo 113, Japan

Caveolae are vesicular organelles that represent an appendage of the plasma membrane. Caveolin, a 21-24-kDa integral membrane protein, is a principal component of caveolae membranes in vivo. Caveolin has been proposed to function as a plasma membrane scaffolding protein to organize and concentrate signaling molecules within caveolae, including heterotrimeric G proteins ( and subunits). In this regard, caveolin interacts directly with G subunits and can functionally regulate their activity. To date, three cDNAs encoding four subtypes of caveolin have been described in vertebrates. However, evidence for the existence of caveolin proteins in less complex organisms has been lacking.

Here, we report the identification, cDNA sequence and genomic organization of the first invertebrate caveolin gene, Cav^ce (for caveolin from Caenorhabditis elegans). The Cav^ce gene, located on chromosome IV, consists of two exons interrupted by a 125-nucleotide intron sequence. The region of Cav^ce that is strictly homologous to mammalian caveolins is encoded by a single exon in Cav^ce. This suggests that mammalian caveolins may have evolved from the second exon of Cav^ce. Cav^ce is roughly equally related to all three known mammalian caveolins and, thus, could represent a common ancestor. Remarkably, the invertebrate Cav^ce protein behaves like mammalian caveolins: (i) Cav^ce forms a high molecular mass oligomer, (ii) assumes a cytoplasmic membrane orientation, and (iii) interacts with G proteins. A 20-residue peptide encoding the predicted G protein binding region of Cav^ce possesses "GDP dissociation inhibitor-like activity" with the same potency as described earlier for mammalian caveolin-1. Thus, caveolin appears to be structurally and functionally conserved from worms to man. In addition, we find that there are at least two caveolin-related genes expressed in C. elegans, defining an invertebrate caveolin gene family. These results establish the nematode C. elegans as an invertebrate model system to study caveolae and caveolin in vivo.

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