Circulation Research, Vol 75, 803-812, Copyright © 1994 by American Heart Association

ARTICLES

Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis

JM Miano, P Cserjesi, KL Ligon, M Periasamy and EN Olson
Department of Biochemistry and Molecular Biology, University of Texas M.D. Anderson Cancer Center, Houston 77030.

We cloned a portion of the mouse smooth muscle myosin heavy chain (SM- MHC) cDNA and analyzed its mRNA expression in adult tissues, several cell lines, and developing mouse embryos to determine the suitability of the SM-MHC promoter as a tool for identifying smooth muscle-specific transcription factors and to define the spatial and temporal pattern of smooth muscle differentiation during mouse development. RNase protection assays showed SM-MHC mRNA in adult aorta, intestine, lung, stomach, and uterus, with little or no signal in brain, heart, kidney, liver, skeletal muscle, spleen, and testes. From an analysis of 14 different cell lines, including endothelial cells, fibroblasts, and rhabdomyosarcomas, we failed to detect any SM-MHC mRNA; all of the cell lines induced to differentiate also showed no detectable SM-MHC. In situ hybridization of staged mouse embryos first revealed SM-MHC transcripts in the early developing aorta at 10.5 days post coitum (dpc). No hybridization signal was demonstrated beyond the aorta and its arches until 12.5 to 13.5 dpc, when SM-MHC mRNA appeared in smooth muscle cells (SMCs) of the developing gut and lungs as well as peripheral blood vessels. By 17.5 dpc, SM-MHC transcripts had accumulated in esophagus, bladder, and ureters. Except for blood vessels, no SM-MHC transcripts were ever observed in developing brain, heart, or skeletal muscle. These results indicate that smooth muscle myogenesis begins by 10.5 days of embryonic development in the mouse and establish SM-MHC as a highly specific marker for the SMC lineage. The SM-MHC promoter should therefore serve as a useful model for defining the mechanisms that govern SMC transcription during development and disease.

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				T. Suzuki, H.-S. Kim, M. Kurabayashi, H. Hamada, H. Fujii, M. Aikawa, M. Watanabe, N. Watanabe, Y. Sakomura, Y. Yazaki, et al. Preferential Differentiation of P19 Mouse Embryonal Carcinoma Cells Into Smooth Muscle Cells : Use of Retinoic Acid and Antisense Against the Central Nervous System–Specific POU Transcription Factor Brn-2 Circ. Res., March 1, 1996; 78(3): 395 - 404. [Abstract] [Full Text]

				L. Li, J. M. Miano, P. Cserjesi, and E. N. Olson SM22{alpha}, a Marker of Adult Smooth Muscle, Is Expressed in Multiple Myogenic Lineages During Embryogenesis Circ. Res., February 1, 1996; 78(2): 188 - 195. [Abstract] [Full Text]

				A. B. Firulli, J. M. Miano, W. Bi, A. D. Johnson, W. Casscells, E. N. Olson, and J. J. Schwarz Myocyte Enhancer Binding Factor-2 Expression and Activity in Vascular Smooth Muscle Cells : Association With the Activated Phenotype Circ. Res., February 1, 1996; 78(2): 196 - 204. [Abstract] [Full Text]

				F. F. Samaha, H. S. Ip, E. E. Morrisey, J. Seltzer, Z. Tang, J. Solway, and M. S. Parmacek Developmental Pattern of Expression and Genomic Organization of the Calponin-h1 Gene J. Biol. Chem., January 5, 1996; 271(1): 395 - 403. [Abstract] [Full Text] [PDF]

				E. Ehler, P. S. Jat, M. D. Noble, S. Citi, and A. Draeger Vascular Smooth Muscle Cells of H-2Kb-tsA58 Transgenic Mice : Characterization of Cell Lines With Distinct Properties Circulation, December 1, 1995; 92(11): 3289 - 3296. [Abstract] [Full Text]

				J. Solway, J. Seltzer, F. F. Samaha, S. Kim, L. E. Alger, Q. Niu, E. E. Morrisey, H. S. Ip, and M. S. Parmacek Structure and Expression of a Smooth Muscle Cell-specific Gene, SM22[IMAGE] J. Biol. Chem., June 2, 1995; 270(22): 13460 - 13469. [Abstract] [Full Text] [PDF]

				R. S. Blank, E. A. Swartz, M. M. Thompson, E. N. Olson, and G. K. Owens A Retinoic Acid–Induced Clonal Cell Line Derived From Multipotential P19 Embryonal Carcinoma Cells Expresses Smooth Muscle Characteristics Circ. Res., May 1, 1995; 76(5): 742 - 749. [Abstract] [Full Text]

				J. A. Carson, R. A. Fillmore, R. J. Schwartz, and W. E. Zimmer The Smooth Muscle gamma -Actin Gene Promoter Is a Molecular Target for the Mouse bagpipe Homologue, mNkx3-1, and Serum Response Factor J. Biol. Chem., December 8, 2000; 275(50): 39061 - 39072. [Abstract] [Full Text] [PDF]

				M. Strobeck, S. Kim, J. C. L. Zhang, C. Clendenin, K. L. Du, and M. S. Parmacek Binding of Serum Response Factor to CArG Box Sequences Is Necessary but Not Sufficient to Restrict Gene Expression to Arterial Smooth Muscle Cells J. Biol. Chem., May 4, 2001; 276(19): 16418 - 16424. [Abstract] [Full Text] [PDF]