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Connective Tissue Cells in Healing Rat Myocardium a Study of Cell Reactions in Rhythmically Contracting Environment

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Connective Tissue Cells in Healing Rat Myocardium a Study of Cell Reactions in Rhythmically Contracting Environment Americanjournal ofPathology, Vol. 134, No. 5, May 1989 Copyright © American Associationt ofPathologists Connective Tissue Cells in Healing Rat Myocardium A Study of Cell Reactions in Rhythmically Contracting Environment Rudolf Vracko,* David Thorning,* and sible for the monophasic myocardial response have not Richard G. Fredericksont been clarified. From the Laboratory Service, VA Medical Center, the Four general explanations have been offered for the Departments ofPathology, * and Biological Structure, lack of restorative myocardial repair: 1) Cardiac myo- University ofWashington School ofMedicine, Seattle, cytes, like neurons, are terminally differentiated cells and Washington cannot divide.67 2) Myocardium, in contrast to skeletal muscle, lacks a sarcolemmal framework necessary for tis- sue reconstruction.4 3) Myocardium, in contrast to skele- To better understand the tendency of myocardium tal muscle, lacks myosatellite cells to serve as sources of to heal by scarring rather than regeneration, the new myocytes.7 4) Overgrowth of nonmuscle cells some- authors examined the responses of connective tis- how prevents cardiac myocyte proliferation.67 Recent sue cells (CTCs) after three types ofnecrotizing in- studies have negated the first two explanations by show- juries. Derived from myocardial interstitial cells, ing that adult mammalian left ventricular myocytes are ca- CTCs proliferated in both the connective tissue pable of DNA synthesis in vivo and in vitro and of cell space and the compartment of necrotic myocytes. division in vitro8"1' and that mammalian myocardium has They assumed various cell forms: fibrocytelike a "sarcolemmal" framework provided by a basal lamina CTCs throughout the sites ofinjury deposited extra- (BL) framework.12 The effects of myosatellite cell absence cellular scar tissue elements, established CTC- myo- is unclear at the present time, and no data are available cyte contacts, and helped anchor myocytes to scar to consider critically the effect of nonmyocyte cell over- tissue with myotendonlike specializations; CTCs growth on the process of myocardial reconstruction. with more complexforms established CTC-myocyte One of the factors unique to myocardium is its need relationships, suggesting important roles in com- to maintain forceful, rhythmic contractions throughout the munication and tissue remodeling. CTCs within healing period. It is obvious that nonlethal necrotizing scar tissue differentiated into myofibrocytes, chon- myocardial injuries interrupt myofiber continuity, that unin- drocytes, and possibly smooth muscle cells. Most jured myocytes must continue contracting, and that the scar tissue elements were disposed in the long axis forces of contraction will act on the site of injury. To our ofmyocytes. These alterations inform indicate that knowledge, the problems associated with wound healing CTCs have various roles in myocardial repair and in an environment of intermittent pulling and stretching suggest that a number of the roles are modulated have not been studied. It has been shown, however, that by contractile forces. (Am J Pathol 1989, 134: intermittent stretching can have a significant effect on the 993-1006) phenotypic expressions of nonmyocardial cells in vitro.13 15 In view of the unresolved issues, we have examined in Like other tissues, myocardium responds to necrotic inju- detail the basic reactions of adult rat left ventricular myo- ries by inflammatory exudation and connective tissue cell cardium to three different types of necrotizing injuries. (CTC) proliferation. Unlike most nonmyocardial tissues, which can heal either by restoration of structure or by scar tissue formation, myocardium seems to be limited to heal- Supported by VA Research Funds and the American Heart Association. ing by scar tissue formation. The tendency to scar and the Accepted for publication January 18, 1989. Address reprint requests to Rudolf Vracko, MD, Laboratory Service structural and some biochemical features of the process (113), VA Medical Center, 1660 South Columbian Way, Seattle, WA have been defined,1-5 however, the mechanisms respon- 98108. 993 994 Vracko, Thorning, and Frederickson AJP May 1989, Vol. 134, No. 5 Based on the need to evaluate stereologically complex closed in two layers. Rats were killed at 1 (N = 10), 4 (N interactions between the elements in necrotic, healing, = 10), 8 (N = 10), 18 (N = 10), and 42 (N = 10) days after and adjacent uninjured sites, we carefully selected tissue injury for light microscopy and at 2 (N = 2), 4 (N = 2), 8 samples oriented in the longitudinal axis of myofiber (N = 2), and 16 (N = 2) hours and 1 (N = 10), 4 (N = 10), chains and those perpendicular to that axis. In earlier re- 7 (N = 10), 14 (N = 10), 28 (N = 10), and 42 (N = 10) ports, we detailed the fate of myocardial BL framework12 days after injury for electron microscopy. and the reactions of myocytes left viable along the edge of injury.i6 In this report, we detail the reactions of connec- tive tissue cells (CTCs). Isoproterenol Injury Our findings suggest that myocardial wound healing is a complex process that involves interactions between The method has been described.19 The animals were myocytes, CTCs, extracellular matrix elements, and phys- given a single intraperitoneal injection of isoproterenol, ical forces. CTCs appear to have multiple roles in the pro- 100 mg/kg body weight. One set was killed 2 (N = 3), 4 cess. They form and fortify scar tissue, help anchor myo- (N = 3), 8 (N = 3), and 16 (N = 3) hours after injury, fibers to scar tissue, and may play a major role in the spa- one animal used for light microscopy, and two for electron tial organization of reparative tissue elements. The microscopy from each interval. Another set was killed at formation of myotendinous junctions, unidirectional spa- 1 (N = 10), 4 (N = 10), 8 (N = 10), 16 (N = 10), 28 (N tial orientation of scar tissue elements, and fortification of = 10), and 42 (N = 10) days after injury, three animals scar tissue by smooth muscle cells and chondrocytes, were used for light and seven for electron microscopy strongly support the notion that myocardial contractions from each interval. are important determinants in the course of myocardial repair. Preparation of Tissue Materials and Methods The excised hearts were perfused retrograde through the ascending aorta from a reservoir located 88 cm above Male and female Sprague-Dawley rats (250 to 300 g) were the heart and kept at room temperature. All hearts were anesthetized for surgical procedures with Metafane prefused first with 15 ml of 0.1% procaine in phosphate- (Methoxyfluorane). Each animal was given 800 units of buffered saline (PBS) to wash out the blood and to stop sodium heparin intravenously minutes before being killed heart contractions. For light microscopy and immunocyto- by Metafane overdose. chemistry, PBS perfusion was followed by perfusion with either 30 ml of periodate-lysine-paraformaldehyde (PLP)20 or 30 ml of 3.5% paraformaldehyde in PBS. For electron Ischemic Injury microscopy, PBS perfusion was followed by perfusion with 100 ml of an osmium mixture described by McCallis- The procedure has been described in detail.17 The left ter and Page.2' chest cavity was entered between the fourth and fifth ribs Tissues for light microscopy were postfixed overnight and the descending branch of the left coronary artery oc- in their respective perfusates. For routine examination, cluded by ligation 2 to 3 mm from its origin. The chest they were embedded in Historesin (LKB, Bromm, Swe- was closed and the animals allowed to recover. Rats were den), sectioned with glass knives at 1.5 , setting, and killed at 1 (N = 2), 2 (N = 2), 4 (N = 2), 6 (N = 2), 14 (N stained with equal volumes of 1 % azure 11 in water and 1 % = 2), and 28 (N = 2) days after injury. For each time inter- methylene blue in 1 % sodium borate. For immunochemi- val, one rat was used for light and one for electron micros- cal examination, they were embedded in low melting point copy. paraffin (55 to 58 C) and cut into 5 u thick sections. For immunoperoxidase preparations, the deparaffin- ized, rehydrated sections were exposed at room tempera- Freeze-Thaw Injury ture to the following: PBS (10 minutes); 0.75% H202 in PBS (30 minutes); PBS (15 minutes); 0.01% pronase in The procedure has been described in detail.'8 The abdo- PBS (20 minutes), PBS (15 minutes), normal serum (1: men was entered through a midline incision, the left lobe 100) and 2% bovine serum albumin in PBS (30 minutes); of the liver deflected, and an aluminum rod, precooled in and primary antibody (12 hours at room temperature) (1: liquid nitrogen, positioned for 10 seconds in contact with 500 HHF35, a muscle-actin-specific monoclonal antibody the diaphragm underlying the heart. The diaphragm re- obtained from Dr. Allen M. Gown, Department of Pathol- mained intact in all instances. The abdominal incision was ogy, University of Washington).22 Controls were reacted Connective Tissue Cells in Healing Myocardium 995 A/PMay 1989, Vol. 134, No. 5 RLi- Figure 1 A. Crossection ofniormal rat myocardiumfixed byperfusion. The capillaries are distended and the connective tissue space uwidened byperfusate. Arrowspoint to the small and inConspicuous connective tissue cells, uwhich tenid to be located near capillaries (X2600). B: Tjpical connective tissufe cell in niormal rat myocardium. The cell has two slender cell extentsionis, one in contact with a cell extension of another connective tissuie cell. The nucleus occupies most of cell volume, anid scanty perinuclear cytoplasm contains maintlyj rouigh endoplasmic reticulum (X 10,000). C: Rat mYocardium 20 hours after isoprotereniol injury. An activated connective tisste cell is located between a viable (V) and a necrotic (N) myocyte. Compared u'ith its counlterpart in (1B), its shape is less angulate, its periniuclear cytoplasm more abundant, its nucleoplasm less conidenised, anid its nucleolus more prominent (X4000). (30 minutes) with nonimmune IgG from the same species isothiocyanite (FITC)-labeled goat anti-rabbit IgG (1:16). and at the same dilution as the primary antibody.
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