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Structure and Function of Connective Tissue in Cardiac Muscle: Collagen Types I and III in Endomysial Struts and Pericellular Fibers

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Structure and Function of Connective Tissue in Cardiac Muscle: Collagen Types I and III in Endomysial Struts and Pericellular Fibers Scanning Microscopy Volume 2 Number 2 Article 33 2-10-1988 Structure and Function of Connective Tissue in Cardiac Muscle: Collagen Types I and III in Endomysial Struts and Pericellular Fibers Thomas F. Robinson Albert Einstein College of Medicine Leona Cohen-Gould Albert Einstein College of Medicine Stephen M. Factor Albert Einstein College of Medicine Mahboubeh Eghbali Albert Einstein College of Medicine Olga O. Blumenfeld Albert Einstein College of Medicine Follow this and additional works at: https://digitalcommons.usu.edu/microscopy Part of the Life Sciences Commons Recommended Citation Robinson, Thomas F.; Cohen-Gould, Leona; Factor, Stephen M.; Eghbali, Mahboubeh; and Blumenfeld, Olga O. (1988) "Structure and Function of Connective Tissue in Cardiac Muscle: Collagen Types I and III in Endomysial Struts and Pericellular Fibers," Scanning Microscopy: Vol. 2 : No. 2 , Article 33. Available at: https://digitalcommons.usu.edu/microscopy/vol2/iss2/33 This Article is brought to you for free and open access by the Western Dairy Center at DigitalCommons@USU. It has been accepted for inclusion in Scanning Microscopy by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. Scanning Microscopy, Vol. 2, No. 2, 1988 (Pages 1005-1015) 0891-7035/88$3.00+.00 Scanning Microscopy International, Chicago (AMF O'Hare), IL 60666 USA STRUCTURE AND FUNCTION OF CONNECTIVE TISSUE IN CARDIAC MUSCLE: COLLAGEN TYPES I and III IN ENDOMYSIAL STRUTS AND PERICELLULAR FIBERS Thomas F. Robinsonl,2 *, Leona Cohen-Gouldl , Stephen M. Factorl,3, Mahboubeh Eghbali4, Olga 0. Blumenfeld4 Departments of 1) Medicine, Cardiovascular Research Laboratories; 2) Physiology & Biophysics; 3) Pathology; and 4) Biochemistry Albert Einstein College of Medicine, Bronx, NY 10461 (Received for publication April 28, 1987, and in revised form February 10, 1988) Abstract Introduction Heart myocytes and capillaries are enmeshed in The large population of variably oriented myo­ a complex array of co nnective tissu e structures ar­ cytes of cardiac muscle are enmeshed in an elaborate ranged in several levels of organization: epimysium, and extensive array of connective tissue. Consid­ the sheath of connective tissue that surrounds mus­ erable research at the level of the light microscope cles; perimysium, which is associated with groups of was performed on myocardia l connective tissue in the cells; and endomysium, which surrounds and intercon­ early part of this century (Holmgren, 1907; nects individual cells. The present paper is a review Benninghoff, 1930), but was followed by several dec­ of work in this field with an emphasis on new, un­ ades of more modest exp loration in this field. How­ published findings, including composition of endo­ ever, within the last decade, interest in the structure mysial fibers and disposition of newly described peri­ and function of myocardial connective tissue has mysial fibers. The role of scanning electron micros­ blossomed, due largely to results achieved with the copy in the development of current understanding is scanning electron microscope and to a consequent also outlined. Biaxially arranged epimysial fibers awareness of the many possible functions of connec­ form a sheath around papillary muscles and trabe­ tive tissue in cardiac physiology and pathophysiology. culae that becomes increasingly well-oriented with (The role of the extracellu l ar matrix in development the muscle axis during stretch. Perimysial structures is a related area of active exploration, but is not are associated with groups of cells, and include covered here; the reader is referred to the mono­ weaves and septa of collagen, tendon-like fibers bet­ graph edited by Zak (1984) for extensive, recent ween weaves, ribbon-like fibers perpendicular to reviews, particularly in avian heart.) myocytes, and the newly described coiled perimysial The myocardial connective tissue, like that in fibers, which form an array in parallel with the skeletal muscle, is generally considered to be organ­ myocytes and the epimysial net. The endomysium in­ ized on three levels. Epimysium is the sheath that cludes struts that bridge cells and pericellular fibers; surrounds the entire muscle, endomysium is the fine both contain collagen types I and III. The evidence connective tissue that surrounds and interconnects for the latter is presented in this paper and depends individual cells, and perimysium is associated with upon the use of antibody localization with fluores­ groups or bundles of cells. cent markers in light microscopy and colloidal gold The present paper contains a brief review of for scanning electron microscopy. The implications published studies that are related to the structure of the composition of collagen fibers for myocardial and function of connective tissue at all three levels function are discussed in relation to intra-cellular of organization in mammalian heart; however, the and other extra-cellular structures. emphasis is on new results related to endomysial s truts and pericellular fibers. Results from several laboratories are reported, including both unpublished results and results in press from the authors' labora­ Key Words: Cardiac muscle, connective tissue , epi­ tories. The extended discussion is aimed at putting mysi um , perimysium, endomysium, collagen, struts, the lat est findings in perspective. elastin, microfibrils, microthreads, antibody locali­ zation, scanning electron microscopy, transmission Abbreviations elec tron microscopy, light microscopy BEi backscattered electron imaging in SEM; CML collagen fibril-microthread-granule lattice; CPF co iled perimysial fibers; DIC = differential interference contrast microscopy; * Address for correspondence: FITC = fluorescein isothiocyanate; Thomas F. Robinson, LM light microscopy; Cardiovascular Research Labs., Forch. G42 PBS phosphate-buffered saline; Albert Einstein College of Medicine SEI secondary electron imaging in SEM; 1300 Morris Park Avenue SEM scanning electron microscopy; Bronx, New York 10461 TEM transmission electron microscopy. Phone No. (212) 430-2609 1005 T.F. Robinson, L. Cohen-Gould, S.M. Factor, et al. Materials and Methods bodies to collagen type I and to collagen type III bind to different protein bands. Tissue preparation Antibody staining and localization Male W1star rats were lightly anesthetized with Samples were labelled with the indirect method. ether and then sacrificed painlessly by cervical dislo ­ Sections were equilibrated in buffer that contained cation, and the hearts quickly removed and placed in Bovine Lacto Transfer Technique Optimizer (BLOTTO) Tyrode's solution (in mM: Na+ 151.3, ca2+ 2.4 , K+ in order to minimize non-specific binding of the an­ 4.0, Mg2+ 0.5, c1- 147.3, HzPO4- 12. 0, and dex trose tibody (Johnson et al. 1984), rinsed in PBS, and then 5.5). incubated with 50 µl of the primary antibody (rabbit Ultrastructure antibody to rat collagen type I or III) at room tem­ Hearts destined for ul trastructural analvsis were perature for 30 min. in a humid chamber. cut open and fixed by immersion in buffered 6% glu­ Samples were rinsed with PBS, drained, and taraldehyde for 3 h at room temperature or overnight then labelled with the second layer in a humid cham­ in the cold. Buffer rinse was followed by dissection ber for 30 min. at room temperature. Second layer of papillary muscles and strips of ventricle wall, then for the samples destined for LM was goat-anti - rabbit post-fixation in 1 % OsO4 for 1 h, followed by buffer IgG labelled with FITC (Miles-Yeda L & D, Rehovot, rinse, and dehydration in a graded ethanol series. Israel). Samples were rinsed with PBS, drained, Samples for TEM were embedded in ERL resin mounted with a solution of 1 part 0. 3 M triethylene­ (Spurr, 1969), stained with uranium and lead salts diamine in 9 parts glycerol, and covered with glass and viewed in a JEOL 100 CX or JEOL 1200 EX. cover slips. Photomicrography was performed with a Samples for SEM were critical point dried in a Zeiss WL microscope fitted with epi- ultraviolet illu­ Samdri 790 (Tousimis Co., Rockville , MD) . Some mination and filters for FITC and rhodamine. samples were viewed after coating with Pd-Au, Kodachrome 400 or Kodak Tri-X film was used. whereas others were immersed in liquid nitrogen , Samples destined for SE M were incubated in a cracked with a pr e-co oled razor blade (Caulfield and humid chamber for 60 min. with a second layer con­ Borg, 1979) , dried by evaporation under vacuum, sisting of goat- anti-rabbit IgG labelled with col­ coated, and viewed in a JSM 25S. loidal gold particles 40 nm. in diameter (Janssen Silver staining Pharmaceutic a, Piscataway, NJ) . Samples were rinsed Hearts were prepared for silver staining by fix­ in PBS, post-fixed in 6% glutaraldehyde for 1/2 hat ation in 3. 7 % phosphat e- buffered formaldehyd e for a t room temperatur e, rinsed, post-fixed in 1% OsO4 in least 2 weeks. Frozen sections, approximately 80 µm buffer for 10 min, rinsed, dehydrated in a graded thick, were cut, floated on distilled water, placed ethanol series, and cr iti ca l point dried in CO2 in a successively in methyl alcohol, Folch' s solution, abso­ Samdri 790 (Tousimis Corp., Rockville, MD). Samples lute methyl alcohol, distilled water, 5 % potassium hy­ were photographed in a JSM 25S in our Analytical droxide, a rinse in running tap water, 1/600 potassi­ Ultrastructure Center. Paired BEI/SEI was perform ­ um permanganate, tap wat er, 5% oxalic acid for ed. Kodak 4127 film was used. bleaching,
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