Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development

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Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development

HS Baldwin, HM Shen, HC Yan, HM DeLisser, A Chung, C Mickanin, T Trask, NE Kirschbaum, PJ Newman, SM Albelda and al. et
Department of Pediatrics, Children's Hospital of Philadelphia, PA 19104.

The establishment of the cardiovascular system represents an early, critical event essential for normal embryonic development. An important component of vascular ontogeny is the differentiation and development of the endothelial and endocardial cell populations. This involves, at least in part, the expression and function of specific cell surface receptors required to mediate cell-cell and cell-matrix adhesion. Platelet endothelial cell adhesion molecule-1 (PECAM-1, CD31) may well serve such a function. It is a member of the immunoglobulin superfamily expressed by the entire vascular endothelium in the adult. It is capable of mediating adhesion by a heterophilic mechanism requiring glycosaminoglycans, as well as by a homophilic, glycosaminoglycan independent, mechanism. It has been shown to regulate the expression of other adhesion molecules on naive T cells. This report documents by RT-PCR and immunohistochemical analysis the expression of PECAM-1 during early post implantation mouse embryo development. PECAM-1 was expressed by early endothelial precursors first within the yolk sac and subsequently within the embryo itself. Interestingly, embryonic PECAM-1 was expressed as multiple isoforms in which one or more clusters of polypeptides were missing from the cytoplasmic domain. The sequence and location of the deleted polypeptides corresponded to exons found in the human PECAM-1 gene. The alternatively spliced isoforms were capable of mediating cell-cell adhesion when transfected into L-cells. The isoforms differed, however, in their sensitivity to a panel of anti-PECAM-1 monoclonal antibodies. These data suggest that changes in the cytoplasmic domain of PECAM-1 may affect its function during cardiovascular development, and are consistent with our earlier report that systematic truncation of the cytoplasmic domain of human PECAM-1 resulted in changes in its ligand specificity, divalent cation and glycosaminoglycan dependence, as well as its susceptibility to adhesion blocking monoclonal antibodies. This is the first report of naturally occurring alternatively spliced forms of PECAM-1 having possible functional implications.

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				H.-J. Byun, I.-K. Hong, E. Kim, Y.-J. Jin, D.-I. Jeoung, J.-H. Hahn, Y.-M. Kim, S. H. Park, and H. Lee A Splice Variant of CD99 Increases Motility and MMP-9 Expression of Human Breast Cancer Cells through the AKT-, ERK-, and JNK-dependent AP-1 Activation Signaling Pathways J. Biol. Chem., November 17, 2006; 281(46): 34833 - 34847. [Abstract] [Full Text] [PDF]

				V. Kriz, N. Agren, C. K. Lindholm, S. Lenell, J. Saldeen, J. Mares, and M. Welsh The SHB Adapter Protein Is Required for Normal Maturation of Mesoderm during in Vitro Differentiation of Embryonic Stem Cells J. Biol. Chem., November 10, 2006; 281(45): 34484 - 34491. [Abstract] [Full Text] [PDF]

				J.-W. Chen, B. Zhou, Q.-C. Yu, S. J. Shin, K. Jiao, M. D. Schneider, H. S. Baldwin, and J. M. Bergelson Cardiomyocyte-Specific Deletion of the Coxsackievirus and Adenovirus Receptor Results in Hyperplasia of the Embryonic Left Ventricle and Abnormalities of Sinuatrial Valves Circ. Res., April 14, 2006; 98(7): 923 - 930. [Abstract] [Full Text] [PDF]

				J. L. Jadrich, M. B. O'Connor, and E. Coucouvanis The TGF{beta} activated kinase TAK1 regulates vascular development in vivo. Development, April 1, 2006; 133(8): 1529 - 1541. [Abstract] [Full Text] [PDF]

				E. M. Morin-Kensicki, B. N. Boone, M. Howell, J. R. Stonebraker, J. Teed, J. G. Alb, T. R. Magnuson, W. O'Neal, and S. L. Milgram Defects in Yolk Sac Vasculogenesis, Chorioallantoic Fusion, and Embryonic Axis Elongation in Mice with Targeted Disruption of Yap65 Mol. Cell. Biol., January 1, 2006; 26(1): 77 - 87. [Abstract] [Full Text] [PDF]

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				P. L. W. Yun, A. A. Decarlo, C. C. Chapple, and N. Hunter Functional Implication of the Hydrolysis of Platelet Endothelial Cell Adhesion Molecule 1 (CD31) by Gingipains of Porphyromonas gingivalis for the Pathology of Periodontal Disease Infect. Immun., March 1, 2005; 73(3): 1386 - 1398. [Abstract] [Full Text] [PDF]

				S. Sinha, M. H. Hoofnagle, P. A. Kingston, M. E. McCanna, and G. K. Owens Transforming growth factor-{beta}1 signaling contributes to development of smooth muscle cells from embryonic stem cells Am J Physiol Cell Physiol, December 1, 2004; 287(6): C1560 - C1568. [Abstract] [Full Text] [PDF]

				A. M. Masino, T. D. Gallardo, C. A. Wilcox, E. N. Olson, R. S. Williams, and D. J. Garry Transcriptional Regulation of Cardiac Progenitor Cell Populations Circ. Res., August 20, 2004; 95(4): 389 - 397. [Abstract] [Full Text] [PDF]

				T. Furusawa, K. Ohkoshi, C. Honda, S. Takahashi, and T. Tokunaga Embryonic Stem Cells Expressing Both Platelet Endothelial Cell Adhesion Molecule-1 and Stage-Specific Embryonic Antigen-1 Differentiate Predominantly into Epiblast Cells in a Chimeric Embryo Biol Reprod, May 1, 2004; 70(5): 1452 - 1457. [Abstract] [Full Text] [PDF]

				D. Feng, J. A. Nagy, K. Pyne, H. F. Dvorak, and A. M. Dvorak Ultrastructural Localization of Platelet Endothelial Cell Adhesion Molecule (PECAM-1, CD31) in Vascular Endothelium J. Histochem. Cytochem., January 1, 2004; 52(1): 87 - 102. [Abstract] [Full Text] [PDF]

				H. Solberg, J. Rinkenberger, K. Dano, Z. Werb, and L. R. Lund A functional overlap of plasminogen and MMPs regulates vascularization during placental development Development, September 15, 2003; 130(18): 4439 - 4450. [Abstract] [Full Text] [PDF]

				T. Ishida, R. K. Kundu, E. Yang, K.-i. Hirata, Y.-D. Ho, and T. Quertermous Targeted Disruption of Endothelial Cell-selective Adhesion Molecule Inhibits Angiogenic Processes in Vitro and in Vivo J. Biol. Chem., September 5, 2003; 278(36): 34598 - 34604. [Abstract] [Full Text] [PDF]

				S. Li, D.-Z. Wang, Z. Wang, J. A. Richardson, and E. N. Olson The serum response factor coactivator myocardin is required for vascular smooth muscle development PNAS, August 5, 2003; 100(16): 9366 - 9370. [Abstract] [Full Text] [PDF]

				P. J. Newman and D. K. Newman Signal Transduction Pathways Mediated by PECAM-1: New Roles for an Old Molecule in Platelet and Vascular Cell Biology Arterioscler. Thromb. Vasc. Biol., June 1, 2003; 23(6): 953 - 964. [Abstract] [Full Text] [PDF]

				C. R. Rosenfeld, C. Chen, T. Roy, and X.-T. Liu Estrogen Selectively Up-Regulates eNOS and nNOS in Reproductive Arteries By Transcriptional Mechanisms Reproductive Sciences, May 1, 2003; 10(4): 205 - 215. [Abstract] [PDF]

				J. Zhu, K. Motejlek, D. Wang, K. Zang, A. Schmidt, and L. F. Reichardt {beta}8 integrins are required for vascular morphogenesis in mouse embryos Development, March 8, 2003; 129(12): 2891 - 2903. [Abstract] [Full Text] [PDF]

				K. E. McGrath, A. D. Koniski, J. Malik, and J. Palis Circulation is established in a stepwise pattern in the mammalian embryo Blood, March 1, 2003; 101(5): 1669 - 1675. [Abstract] [Full Text] [PDF]

				D. Ilic, B. Kovacic, S. McDonagh, F. Jin, C. Baumbusch, D. G. Gardner, and C. H. Damsky Focal Adhesion Kinase Is Required for Blood Vessel Morphogenesis Circ. Res., February 21, 2003; 92(3): 300 - 307. [Abstract] [Full Text] [PDF]

				J. M. Enciso, D. Gratzinger, T. D. Camenisch, S. Canosa, E. Pinter, and J. A. Madri Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2 J. Cell Biol., February 18, 2003; 160(4): 605 - 615. [Abstract] [Full Text] [PDF]

				J. M. Ricono, Y.-C. Xu, M. Arar, D.-c. Jin, J. L. Barnes, and H. E. Abboud Morphological Insights into the Origin of Glomerular Endothelial and Mesangial Cells and Their Precursors J. Histochem. Cytochem., February 1, 2003; 51(2): 141 - 150. [Abstract] [Full Text] [PDF]

				H. Hirai, M. Ogawa, N. Suzuki, M. Yamamoto, G. Breier, O. Mazda, J. Imanishi, and S.-I. Nishikawa Hemogenic and nonhemogenic endothelium can be distinguished by the activity of fetal liver kinase (Flk)-1 promoter/enhancer during mouse embryogenesis Blood, February 1, 2003; 101(3): 886 - 893. [Abstract] [Full Text] [PDF]

				H. Matsumoto, W.-g. Ma, T. Daikoku, X. Zhao, B. C. Paria, S. K. Das, J. M. Trzaskos, and S. K. Dey Cyclooxygenase-2 Differentially Directs Uterine Angiogenesis during Implantation in Mice J. Biol. Chem., August 2, 2002; 277(32): 29260 - 29267. [Abstract] [Full Text] [PDF]