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Expression of Multiple Gap Junction Proteins in Human Fetal and Infant Hearts

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Expression of Multiple Gap Junction Proteins in Human Fetal and Infant Hearts 0031-399819413605-0561$03.00/0 PEDIATRIC RESEARCH Vol. 36, No. 5, 1994 Copyright O 1994 International Pediatric Research Foundation, Inc. Printed in U.S.A. Expression of Multiple Gap Junction Proteins in Human Fetal and Infant Hearts SU-CHIUNG CHEN, LLOYD M. DAVIS, EILEEN M. WESTPHALE, ERIC C. BEYER,~ AND JEFFREY E. SAFFITZ Departments of Pathology [J.E. S. Medicine [J.E. S.], and Pediatrics [L.M. D., E. M. W., E. C. B.], Washington University School of Medicine, and Department of Pediatrics [S.C.], St. Louis University School of Medicine, St. Louis, Missouri 63110 Mammalian cardiac myocytes express multiple gap different developmental stages analyzed. Immunofluores- junction channel proteins or connexins. Expression pat- cence identified abundant Cx43 in the known distribution terns of the avian homologues of the mammalian cardiac of gap junctions in myocytes in sections of all hearts. Cx45 connexins change during cardiac morphogenesis in associ- staining was inconspicuous in fetal hearts but was readily ation with changes in the electrophysiologic properties of apparent in cardiac myocytes in hearts of older subjects. In intercellular junctions in chick cardiac myocytes. To de- contrast, Cx40 staining in the ventricle was confined to termine whether expression of cardiac connexins is devel- mural coronary arteries, apparently in endothelial cells, opmentally regulated in humans, we characterized con- whereas in the atrium (2x40 staining at myocyte junctions nexin mRNA and protein content and distribution in hearts was abundant. Junctions in hypertrophied myocardium of of 11 human fetuses (74 to 122 d gestational age), seven children with congenital or acquired heart disease appeared children (0.5 mo to 3 y of age), and two adults. Northern more prominent and complex than in normal tissues. Thus, blot analysis identified transcripts of connexin40 (Cx40), the human heart contains multiple connexins, but their connexin43 (Cx43), and connexin45 (-45) genes in all distribution and developmental patterns differ from each hearts analyzed. Cx40 mRNA was approximately 5-fold other and from those in other species. Cx45 expression is more abundant in samples from fetal hearts than in hearts not restricted to the fetal human heart. Cx40 expression in of children or adults. However, fetal samples used for ventricles occurs selectively in coronary arteries. (Pediatr RNA extraction included atrial as well as ventricular myo- Res 36: 561-566, 1994) cardium, whereas samples from children and adults were exclusively ventricular. Northern analysis of adult human right atrial appendages revealed abundant Cx40 mRNA, Abbreviations thus suggesting that the greater amount of Cx40 signal seen Cx40, connexin40 on Northern blots from fetal hearts could have been attrib- Cx43, connexin43 utable to atrial contributions. Neither Cx43 nor Cx45 Cx45, connexin45 mRNA varied significantly in amount in samples from the pS, picosiemen Mammalian cardiac myocytes express at least three and the nodes and bundles of the cardiac conduction distinct gap junction channel proteins (1). These proteins, system may be attributable, in part, to different patterns Cx40, Cx43, and Cx45, form channels with unique bio- of connexin expression. physical properties (2). In adult hearts, different cardiac Expression of the avian homologues of these connex- tissues having different conduction properties have been ins changes during chick cardiac morphogenesis (9). Ex- found to express distinct connexin phenotypes (3-8), pression of Cx45 appears to be highly regulated during suggesting that the disparate electrophysiologic proper- embryonic development in chicks. Cx45 mRNA is abun- ties that distinguish atrial and ventricular myocardium dant in hearts from 6-d-old chick embryos but is much less abundant in later developmental stages and is ex- pressed minimally in the adult chicken heart (9). Record- Received February 1, 1994; accepted May 27, 1994. Correspondence and reprint requests: Jeffrey E. Saffitz, M.D., Ph.D., Depart- ings of gap junction channels expressed in communica- ment of Pathology, Box 8118, Washington University School of Medicine, 660 S. tion-deficient cells transfected individually with the three Euclid Ave., St. Louis, MO 63110. cardiac connexins revealed distinct biophysical proper- Supported by National Institutes of Health Grants HJ-45466, HL17647, and HL36773. ties including unitary conductances and voltage depen- 'E.C.B. is an Established Investigator of the American Heart Association. dence (2). For example, mammalian Cx40 and its chick 562 CHEN ET AL. homologue, Cx42, form channels with large unitary con- tricular sample from a patient who underwent repair of ductances (predominately 121 or 158 pS) (2, 10, ll), tetralogy of Fallot, and a sample of left ventricle obtained whereas channels made by Cx43 have a predominant from a cardiac allograft that was excised from a 1-y-old unitary conductance of 44 pS (2). Cx45 channels have patient at the time of retransplantation because of acute unitary conductances of only approximately 30 pS (2). rejection. Samples of left ventricular myocardium were These observations suggest that junctional conductance also obtained at autopsy within 2 h of death in a 5-mo-old in cardiac myocytes that express multiple connexins de- child who died of idiopathic dilated cardiomyopathy and pends, in part, on the relative abundance of channels a 3-y-old normal child who died of head injury sustained formed by each of the three proteins. This hypothesis is in a motor vehicle accident. Adult left ventricular sam- supported by observations that the electrophysiologic ples were obtained from a 38-y-old patient with dilated properties of intercellular junctions in chick cardiac myo- cardiomyopathy who was undergoing heart transplanta- cytes change during development in a pattern consistent tion and a 33-y-old trauma victim with no history of heart with the known changes in connexin phenotype expres- disease. All of the left ventricular samples from pediatric sion (2). There have been some descriptions of changes in and adult hearts were divided into multiple portions, expression of Cx43 mRNA and protein in the developing frozen rapidly, and stored at -70°C until used in immu- rodent heart (12-14). However, neither Cx40 nor Cx45 nofluorescence and Northern blot analyses. has been examined in the developing mammalian heart. Northern blot analysis. Total cellular RNA was prepared Expression of cardiac connexins in human fetal and from the combined atrial and ventricular myocardium of infant myocardium has not been characterized previ- fetal hearts and ventricular myocardium of pediatric and ously, nor have the effects of myocardial disease on adult hearts using the guanidinium isothiocyanate- connexin expression been fully explored. Moreover, con- phenol-chloroform extraction method (15) as previously siderable species variation may exist in connexin expres- described (1). An additional study was performed to sion patterns (3-8). Thus, observations in chick and ro- compare the relative abundance of Cx40 transcripts in dent hearts may not be applicable to human myocardium. RNA isolated from the right atrial appendage and left Accordingly, the present study was performed to char- ventricle of two other adults (aged 54 and 66 y). Each lane acterize expression of cardiac connexins in human fetal was loaded with 10 pg of RNA except for the membrane and infant hearts and to determine whether expression of probed with Cx45, in which each lane contained 20 pg of cardiac connexins is developmentally regulated or al- RNA. The amount of RNA transferred to each lane of the tered in myocardial disease. nylon membranes was determined by visual assessment under UV light of gels and membranes stained with METHODS ethidium bromide. Approximately equal amounts of RNA were loaded and transferred as judged by this Tissue acquisition. Myocardial samples from 20 human criterion. hearts were analyzed. These included samples from 11 Membranes containing RNA from fetal, pediatric, and fetuses (74 to 122 d gestational age), seven children (0.5 adult hearts were hybridized with 32~-labeledDNA mo to 3 y of age), and two adults. Fetal hearts were probes corresponding to human Cx40, rat Cx43, or hu- obtained from the Central Laboratory for Human Em- man Cx45 as previously described (16). Human Cx43 has bryology at the University of Washington, Seattle, in been cloned and sequenced, and it shares more than 97% accordance with U. S. Public Health Service guidelines amino acid sequence homology to rat Cx43 (16, 17). In on research using human fetal tissue. These cardiac sam- previous studies, we have found that the 32~-labeled ples were collected from conceptal tissues, snap frozen, DNA probes hybridize specifically under stringent con- and shipped to our laboratory on dry ice. Upon arrival, a ditions with their respective mRNA obtained from human small fragment of the left ventricle was removed from the myocardium (16). frozen sample and stored at -70°C for subsequent prep- Probes were labeled with 32~using random hexanucle- aration of frozen sections and immunofluorescence anal- otide primers and the Klenow fragment of DNA polymer- ysis. The remainder of the sample was divided into two ase I as described (1). Standard hybridization conditions approximately equal portions, and each was subse- with stringent washes were used for all blots. Positive quently used for preparation of total tissue RNA and Northern blot analyses were confirmed in two additional Northern
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