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Role of Extracellular Matrix in Regulating Embryonic Epithelial-Mesenchymal Transition

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Role of Extracellular Matrix in Regulating Embryonic Epithelial-Mesenchymal Transition BioMol Concepts, Vol. 3 (2012), pp. 333–344 • Copyright © by Walter de Gruyter • Berlin • Boston. DOI 10.1515/bmc-2011-0065 Review Role of extracellular matrix in regulating embryonic epithelial-mesenchymal transition Francesca Zito considerable amount of data about its basic mechanisms. Istituto di Biomedicina e Immunologia Molecolare From a clinical viewpoint, the results obtained so far offer ‘ Alberto Monroy ’ , Consiglio Nazionale delle Ricerche, a great promise for the development of new therapies. At Via Ugo La Malfa 153, I-90146 Palermo , Italy the same time, they advance our knowledge about essential developmental processes. e-mail: [email protected] Although EMT is a widely studied topic, it is likely that not all aspects of this process have been elucidated so far. Considerable knowledge has been accumulated regarding cell Abstract morphological changes, and the regulation of several genes and various signaling pathways have been partially under- Embryogenesis and morphogenesis are characterized by stood. Still, little is known about the role of the extracellular complex cell rearrangements and movements which require matrix (ECM) as a cell substrate during EMT, and cell motility appropriate interactions of cells with the surrounding extracel- is probably the least understood aspect of the whole process. lular matrix (ECM) by means of specifi c membrane receptors. Many events in developing embryo are associated with Interest in the identifi cation and purifi cation of ECM com- cell migration, which consists of the coordinated move- ponents, as well as in conducting functional studies of them, ments of several different cells over short or long distances including their ligands and other molecules involved in cell- throughout the embryo. The molecular mechanisms under- matrix adhesion, has intensifi ed in recent years, increasing our lying cell migration seem to be similar among different cell knowledge of developmental machinery. Cellular movements types, and the major actors appear to be functionally con- play an important role during the epithelial-mesenchymal served in evolution. Signifi cant progresses in understand- transition (EMT) events, which are key processes in normal ing the basic principles of cell migration have been made, embryogenesis as well as in pathological conditions, such as primarily through studies of in vitro cell cultures in which fi brotic diseases and cancer. Thus, to more fully understand cells usually move on two-dimensional surfaces. During mechanisms underlying the EMT process, and for better knowl- embryogenesis, however, cells migrate through a three- edge of the embryonic defects related to this process, it would dimensional (3D) network of the ECM which possesses dis- be useful to study the substrates on which EMT cells move dur- tinctive physical and chemical properties, thus introducing ing embryo development. This review focuses on a few differ- additional levels of complexity to the system. Cell-ECM ent embryonic systems, taking into account the cell migration interactions, as well as ECM deposition and assembly, are that occurs during EMT and highlighting, in particular, studies essential to shaping the developing embryo and to support- describing the direct involvement of ECM molecules. ing cell polarization, short- and long-range cell migrations, and modifi cations in cell behavior. Keywords: basement membrane; cell migration; heart A link among embryonic EMT, cell movements, and ECM development; neural crest; sea urchin embryo. molecules underlying these movements has rarely been emphasized in the recent literature. Indeed, many issues Introduction remain unresolved, such as: (i) what signals initiate cell move- ments; (ii) how cells undergoing EMT ‘ move across ’ the base- The developing embryo undergoes a highly complex ment membrane; (iii) which ECM molecules are involved; sequence of events devoted to generating the adult body. and (iv) what role they have, and so on. An understanding Among such events, epithelial-mesenchymal transition of basic mechanisms underlying embryonic EMT, the iden- (EMT) is a key embryological process driving the remod- tifi cation and characterization of embryonic cell-ECM adhe- eling of epithelial layers by converting steady-state cells sion molecules, and the growing understanding of their role into individual and motile mesenchymal cells. From a during EMT in many different systems will certainly provide single-layered epithelial embryo, this process produces a answers to many of these questions. three-germ-layered organism with an external ectoderm Details of EMT processes will not be extensively addressed and internal mesoderm and endoderm which will give rise in this review; rather, the purpose is to focus on the cell to tissues and organs. EMT also plays a crucial role in migration during EMT in a few different embryonic sys- pathogenesis, occurring in fi brotic diseases as well as in tems, with special emphasis on those studies which describe cancer progression. Thus, for obvious reasons, numerous the direct involvement of ECM molecules in EMT. Due to studies are currently focused on EMT and are providing a space restrictions, citations primarily refer to key original 334 F. Zito articles or to review articles with more extensive and relevant and positional information. In fact, the fundamental knowl- bibliographies. edge that has emerged in recent years is the active role of ECM molecules in infl uencing (sometimes simultaneously) many aspects of cellular behavior, including cell shape and ECM and embryonic development: a few general polarization, cell motility, cytoskeleton organization, cell pro- concepts liferation and differentiation (4 – 6) . Rozario and DeSimone propose a conception of the ECM as a ‘ morphogenetic lan- Research on ECM molecules and their interactions with liv- guage or code ’ that is interpreted by cells in contact with it ing cells is fundamental for many different disciplines, such (6) . These ECM functions are carried out by at least three as developmental biology, cancer research, and tissue engi- different mechanisms, involving: (i) the composition of the neering. The wide range of syndromes resulting from genetic ECM; (ii) cell surface receptors (briefl y described in a follow- abnormalities of ECM proteins demonstrates the great impor- ing section); and (iii) interactions with soluble growth factors tance of the ECM for normal living cells (1) . to regulate their distribution, activation, and presentation to The ECM is a multifunctional ‘ meshwork of fi bers embed- cells (7) . ded in a gel-like ground substance ’ (2) , whose components are One of the current goals of developmental biologists is synthesized by the resident cells of each tissue and secreted to understand, through various approaches, how ECM mol- via exocytosis. ecules accomplish all these functions. As underlined by It seems diffi cult in this context to delineate a single model Dorothy Hodgkin (Nobel Prize in Chemistry, 1964), ‘ knowl- for the structure of the ECM. In fact, the composition of the edge of structure is critical to an understanding of function. ’ ECM is highly variable among tissues and organs due to a Thus, the identifi cation of ECM molecules and their charac- number of factors, including the presence of multiple forms terization, both at the biochemical and molecular levels, is the of individual molecules and the expression of several mol- fi rst step to be taken. Then, it is important to localize them in ecules in different tissues (2) . Moreover, the physical status of whole-mount embryos and to study their role in vivo , through the ECM varies at different stages of development; its com- functional assays, such as perturbation with specifi c antibod- position is modifi ed, either enzymatically or non-enzymati- ies or molecular probes, or the more sophisticated approach cally, and remodeled in its 3D organization (both in terms of of generating mutant embryonic strains. Although the in vivo architecture and density), thus forming many different natural functional assays have signifi cantly advanced our understand- ‘ scaffolds ’ upon which embryonic cells can organize them- ing of the role of the ECM in developmental processes, care selves in order to build tissues and organs. However, in a very should be taken in interpreting ECM loss-of-function pheno- general way, we can state that the ECM primarily exists in two types. Multiple processes may be compromised due to the forms: as an interstitial matrix fi lling the intercellular space, multifunctional role of single ECM components, and the per- and as the more specialized basement membrane, a thin layer turbation of one element can sometimes induce a cascade of of ECM underlying an epithelium. changes involving more than one molecule. Thus, especially The major structural and functional components of the in mutant embryos with complex phenotypes, more in-depth ECM are fi brillar and non-fi brillar collagens, glycoproteins, analyses are required to obtain extensive descriptions of the proteoglycans, and glycosaminoglycans. Each class of these function of a disrupted gene (8) . molecules has characteristic structures and functions (2, 3) . Collagens are a heterogeneous class of proteins which are the most abundant in the vertebrate body. In addition to being the EMT during embryonic development: a general main structural scaffold of most types of ECM, forming long overview cable-like structures (fi brillar collagens) or mesh-like struc- tures (non-fi brillar collagens), collagens play
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