Effects of mast cells on the behavior of isolated heart fibroblasts: Modulation of collagen...

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JOURNAL OF CELLULAR PHYSIOLOGY 191:51±59 2002) DOI 10.1002/jcp.10071 Effects of Mast Cells on the Behavior of Isolated Heart Fibroblasts: Modulation of Collagen Remodeling and Gene Expression ANGELA DE ALMEIDA, 1 DEANNA MUSTIN, 1 MARY F. FORMAN, 2 GREGORY L. BROWER, 2 JOSEPH S. JANICKI, 2 AND WAYNE CARVER 1 * 1 Department of Developmental Biology and Anatomy, School of Medicine, University of South Carolina, Columbia, South Carolina 2 Department of Anatomy, Physiology, and Pharmacology, School of Veterinary Medicine, Auburn University, Auburn, Alabama The extracellular matrix plays a critical role in the development and maintenance of the vertebrate heart. Changes in the accumulation, composition, or organiza- tion of the extracellular matrix are known to deleteriously affect heart function. Mast cells are thought to stimulate collagen expression and ®broblast proliferation accompanying ®brosis in some organs; however, the effects of mast cells on the heart interstitium are largely unexplored. The present studies were carried out to determine the effects of mast cells on isolated heart ®broblasts. Several in vitro assays were used including collagen gel contraction to examine the effects of mast cells on the function of isolated ®broblasts. Neonatal heart ®broblasts were cultured either with mast cells, mast cell-conditioned medium, or mast cell ex- tracts, and their ability to contract collagen gels measured. Results from these experiments indicated that mast cells inhibit heart ®broblast migration and contraction of 3-dimensional collagen gels. Further experiments indicated that incubation of neonatal heart ®broblasts with extracts of mast cells altered the expression of collagen, matrix metalloproteases, and matrix receptors of the integrin family. These studies suggest that mast cells play an important role in the regulation of the cardiac interstitial matrix. Further studies are warranted to determine the mechanisms whereby mast cells modulate ®broblast activity. J. Cell. Physiol. 191: 51±59, 2002. ß 2002 Wiley-Liss, Inc. The extracellular matrix ECM) of the heart forms a stress-tolerant network that is essential for the proper function of the ventricular myocardium. Alterations in the accumulation and organization of the ECM have been shown concurrent with a number of cardiovascular diseases. These changes in the ECM are thought to deleteriously affect myocardial function. A diverse array of biological factors including transforming growth factor-b, angiotensin II and others have been identi®ed which modulate the expression and organization of ECM components for reviews Carver et al., 1995b, 1999). However, questions remain regarding the sources) of these chemical factors in the developing or diseased heart. That is, are these factors largely systemic or are they locally produced within the heart tissue? Several studies have indicated that mast cells are involved in the modulation of ECM synthesis and accu- mulation in several ®brotic tissues. Increased numbers of mast cells have been shown concurrent with ®brosis of several organs Atkins, 1987; Ruoss and Caughey, 1995). Recent studies have demonstrated that mast cell co-culture or mast cell secretory products affect collagen production and proliferation of dermal ®bro- blasts Carins and Walls, 1997; Kendall et al., 1997). Interestingly, mast cell numbers are increased in the heart concurrent with normal growth and with disease processes Patella et al., 1998); however, little is known about the effects of mast cells or mast cell products on the ventricular interstitium. The present studies were carried out to determine the effects of mast cells on the production of and interaction with ECM by heart ®broblasts. The results demonstrate that co-culture of isolated heart ®broblasts with mast cells or mast cell extracts inhibited the ®broblast mig- ration in and contraction of 3-dimensional collagen gels. Incubation of heart ®broblasts with mast cells also altered the expression of collagen, matrix metallopro- teases, and ECM receptors of the integrin family. These data indicate that mast cells alter ECM expression and ß 2002 WILEY-LISS, INC. Contract grant sponsor: NIH; Contract grant number: HL62228. *Correspondence to: Wayne Carver, Department of Developmen- tal Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29208. E-mail: [email protected] Received 7 May 2001; Accepted 15 October 2001

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