Summary
The cytotrophoblastic cell columns and trophoblastic shell of macaque placentas accumulate progressively greater amounts of intercellular material during early gestation. We studied the composition of this material in placentas collected from 22–34 days of gestation by using immunoperoxidase techniques directed to the extracellular matrix molecules fibronectin, type IV collagen, and laminin. These antigens co-localized within the intercellular deposits at all stages studied. At day 22 the proximal cell columns were composed of cells with narrow interstices and which lacked immunoreactivity for the 3 antigens. Distally the cells were vacuolated and the intercellular spaces increased in size and contained dense matrix deposits. The trophoblastic shell consisted of closely packed, non-vacuolated cytotrophoblast cells with only a delicate meshwork of matrix. By day 27 the matrix deposits of the distal cell columns increased markedly in size. The trophoblastic shell contained larger numbers of vacuolated cells and was occupied by accumulations of matrix. By 34 days the matrix deposits of the cell columns expanded substantially along the longitudinal axes of the columns. These deposits were often continuous with a matrix-dense, cell-deficient layer in the trophoblastic shell. This matrix-rich zone lay between a cellular layer adjacent to the intervilous space and a similar, but discontinuous, cell layer that formed the junctional zone with the endometrium.
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References
Armant DR, Kaplan HA, Lennarz WJ (1986) Fïbronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts. Dev Biol 116:519–523
Autio-Harmainen H, Sandberg M, Pihlajaniemi T, Vuorio E (1991) Synthesis of laminin and type IV collagen by trophoblastic cells and fibroblastic stromal cells in the early human placenta. Lab Invest 64:483–491
Barsky SH, Rao NC, Restrepo C, Liotta L (1984) Immunocytochemical enhancement of basement membrane antigens by pepsin: applications in diagnostic pathology. Am J Clin Pathol 82:191–194
Benirschke K, Kaufmann P (1990) Pathology of the Human Placenta, 2nd edn. Springer, New York
Bischof P, Friedli E, Martelli M, Campana A (1991) Expression of extracellular matrix-degrading metalloproteinases by cultured human cytotrophoblast cells: effects of cell adhesion and immunopurification. Am J Obstet Gynecol 165:1791–1801
Boyd JD, Hamilton WJ (1967) Development and structure of the human placenta from the end of the 3rd month of gestation. J Obstet Gynaecol Br Commonw 74:161–226
Boyd JD, Hamilton WJ (1970) The Human Placenta, Heffer, Cambridge
Carson DD, Tang J-P, Gay S (1988) Collagens support embryo attachment and outgrowth in vitro: effects of the arg-gly-asp sequence. Dev Biol 127:368–375
Damsky CH, Fitzgerald ML, Fisher SJ (1992) Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 89:210–222
Earl U, Estlin C, Bulmer JN (1990) Fibronectin and laminin in the early human placenta. Placenta 11:223–231
Emonard H, Christiane Y, Smet M, Grimaud JA, Foidart JM (1990) Type IV and interstitial collagenolytic activities in normal and malignant trophoblastic cells are specifically regulated by the extracellular matrix. Invas Metast 10:170–177
Feinberg RF, Kao L-C, Haimowitz JE, Queenan JT, Wun T-C, Strauss III JF, Kliman HJ (1989) Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. Lab Invest 61:20–26
Feinberg RF, Kliman HJ, Lockwood CJ (1991) Is oncofetal fibronectin a trophoblast glue for human implantation? Am J Pathol 138:537–543
Fernandez PL, Merino MJ, Nogales FF, Charonis AS, Stetler-Stevenson W, Liotta L (1992) Immunohistochemical profile of basement membrane proteins and 72 kilodalton type IV collagenase in the implantation placental site. Lab Invest 66:572–579
Fisher SJ, Cui T-Y, Zhang L, Hartman L, Grahl K, Gou-Yang Z, Tarpey J, Damsky CH (1989) Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 109:891–902
Furcht LT, McCarthy JB, Palm SL, Basara ML, Enenstein J (1984) Peptide fragments of laminin and fibronectin promote migration (haptotaxis and chemotaxis) of metastatic cells. In: Porter R, Whelen J (eds) Basement Membranes and Cell Movement, Ciba Foundation Symposium No. 108, Pitman, London, pp 130–145
Graham CH, Lala PK (1991) Mechanism of control of trophoblast invasion in situ. J Cell Physiol 148:228–234
Grosser O (1925) Über Fibrinoid in der Placenta. Zeitschr Anat Entw 76:304–314
Kao L-C, Caltabiano S, Wu S, Strauss III JF, Kliman HJ (1988) The human villous cytotrophoblast: interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation. Dev Biol 130:693–702
King BF, Mais JJ (1982) Development changes in rhesus monkey placental villi and cell columns. Anat Embryol 165:361–376
Kitten GT, Markwald RR, Bolender DL (1987) Distribution of basement membrane antigens in cryopreserved early embryonic hearts. Anat Rec 217:379–390
Kliman HJ, Feinberg RF (1990) Human trophoblast-extracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity. Proc Natl Acad Sci USA 87:3057–3061
Kliman HJ, Coutifaris C, Feinberg RF, Strauss III JF, Haimowitz JE (1989) Implantation: in vitro models utilizing human tissues. In: Yoshinaga K (ed) Blastocyst Implantation. Adams, Boston, pp 83–91
Korhonen M, Ylänne J, Laitinen L, Cooper HM, Quaranta V, Virtanen I (1991) Distribution of the α1—α6 integrin subunits in human developing and term placenta. Lab Invest 65:347–356
Leu F-J, Damjanov I (1988) Protease treatment combined with immunohistochemistry reveals heterogeneity of normal and neoplastic basement membranes. J Histochem Cytochem 36:213–220
Librach CL, Werb Z, Fïtzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ (1991) 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 113:437–449
Linask KK, Lash JW (1986) Precardiac cell migration: fibronectin localization at mesoderm-endoderm interface during directional movement. Dev Biol 114:87–101
Little CD, Piquet DM, Davis LA, Walters L, Drake CJ (1989) Distribution of laminin, collagen type IV, collagen type I, and fibronectin in chicken cardiac jelly/basement membrane. Anat Rec 224:417–425
Loke YW, Gardner L, Burland K, King A (1989) Laminin in human trophoblast-decidua interaction. Human Reprod 4:457–463
McCarthy JB, Furcht LT (1984) Laminin and fibronectin promote the haptotactic migration of B16 mouse melanoma cells in vitro. J Cell Biol 98:1474–1480
McCarthy JB, Hagen ST, Furcht LT (1986) Human fibronectin contains distinct adhesion- and motility-producing domains for metastatic melanoma cells. J Cell Biol 102:179–188
Mjaatvedt CH, Lepera RC, Markwald RR (1987) Myocardial specificity for initiating endothelial-mesenchymal cell transition in embryonic chick heart correlates with a particulate distribution of fibronectin. Dev Biol 119:59–67
Moll UM, Lane BL (1990) Proteolytic activity of first trimester human placenta: localization of interstitial collagenase in villous and extravillous trophoblast. Histochemistry 94:555–560
Paulsson M (1992) Basement membrane proteins: structure, assembly, and cellular interactions. Crit Rev Biochem Molec Biol 27:93–127
Puistola U, Rönnberg L, Martikainen H, Turpeenniemi-Hujanen T (1989) The human embryo produces basement membrane collagen (type IV collagen)-degrading protease activity. Human Reprod 4:309–311
Queenan JT, Kao L-C, Arboleda CE, Ulloa-Aguirre A, Golos TG, Cines DB, Strauss JF III (1987) Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts. J Biol Chem 262:10903–10906
Riggot MJ, Moody SA (1987) Distribution of laminin and fibronectin along peripheral trigeminal axon pathways in the developing chick. J Comp Neurol 258:580–596
Rogers SL, Edson KJ, Letourneau PC, McLoon SC (1986) Distribution of laminin in the developing peripheral nervous system of the chick. Dev Biol 113:429–435
Ruoslahti E (1991) Integrins as receptors for extracellular matrix. In: Hay ED (ed) Cell Biology of Extracellular Matrix. Plenum, New York, London, pp 343–363
Sanes JR, Engvall E, Butkowski R, Hunter DD (1990) Molecular heterogeneity of basal laminae: isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J Cell Biol 111:1685–1699
Sinning AR, Krug EL, Markwald RR (1992) Multiple glycoproteins localize to a particulate form of extracellular matrix in regions of the embryonic heart where endothelial cells transform into mesenchyme. Anat Rec 232:285–292
Solursh M, Jensen KL (1988) The accumulation of basement membrane components during the onset of chondrogenesis and myogenesis in the chick wing bud. Development 104:41–49
Sutherland AE, Calarco PG, Damsky CH (1988) Expression and function of cell surface extracellular matrix receptors in mouse blastocyst attachment and outgrowth. J Cell Biol 106:1331–1348
Ulloa-Aguirre A, August AM, Golos TG, Kao L-C, Sukuragi N, Kliman HJ, Strauss III JF (1987) 8-Bromo-adenosine 3′,5′-monophosphate regulates expression of chorionic gonadotropin and fibronectin in human cytotrophoblasts. J Clin Endocrinol Metab 64:1002–1009
Wewer UM, Faber M, Liotta LA, Albrechtsen R (1985) Immunochemical and ultrastructural assessment of the nature of the pericellular basement membrane of human decidual cells. Lab Invest 53:624–633
Wewer UM, Taraboletti G, Sobel ME, Albrechtsen R, Liotta LA (1987) Role of laminin receptor in tumor cell migration. Cancer Res 47:5691–5698
Wilkin PG (1965) Organogenesis of the human placenta. In: De-Haan RL, Ursprung H (eds) Organogenesis. Holt, Rinehart and Winston, New York, pp 743–769
Wislocki GB, Bennett HS (1943) The histology and cytology of the human and monkey placenta, with special reference to the trophoblast. Am J Anat 73:335–449
Wislocki GB, Streeter GL (1938) On the placentation of the macaque (Macaca mulatta), from the time of implantation until the formation of the definitive placenta. Contrib Embryol 27:1–66
Woessner JF (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5:2145–2154
Yagel S, Parhar RS, Jeffrey JJ, Lala PK (1988) Normal nonmetastatic human trophoblast cells share in vitro invasive properties of malignant cells. J Cell Physiol 136:455–462
Yagel S, Kerbel R, Lala P, Eldar-Gera T, Dennis JW (1990) Basement membrane invasion by first trimester human trophoblast: requirement for branched complex-type Asn-linked oligosaccharides. Clin Exp Metast 8:305–317
Yamada T, Isemura M, Yamaguchi Y, Munakata H, Hayashi N, Kyogoku M (1987) Immunohistochemical localization of fibronectin in the human placentas at their different stages of maturation. Histochemistry 86:579–584
Yamaguchi Y, Isemura M, Yosizawa Z, Kurosawa K, Yoshinaga K, Sato A, Suzuki M (1985) Changes in the distribution of fibronectin in the placenta during normal human pregnancy. Am J Obstet Gynecol 152:715–718
Zhou FC (1990) Four patterns of laminin-immunoreactive structure in developing rat brain. Dev Brain Res 55:191–201
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Blankenship, T.N., Enders, A.C. & King, B.F. Distribution of laminin, type IV collagen, and fibronectin in the cell columns and trophoblastic shell of early macaque placentas. Cell Tissue Res 270, 241–248 (1992). https://doi.org/10.1007/BF00328009
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DOI: https://doi.org/10.1007/BF00328009