Extravasation of leukocytes in comparison to tumor cells

The multi-step process of the emigration of cells from the blood stream through the vascular endothelium into the tissue has been termed extravasation. The extravasation of leukocytes is fairly well characterized down to the molecular level, and has been reviewed in several aspects. Comparatively little is known about the extravasation of tumor cells, which is part of the hematogenic metastasis formation. Although the steps of the process are basically the same in leukocytes and tumor cells, i.e. rolling, adhesion, transmigration (diapedesis), the molecules that are involved are different. A further important difference is that leukocyte interaction with the endothelium changes the endothelial integrity only temporarily, whereas tumor cell interaction leads to an irreversible damage of the endothelial architecture. Moreover, tumor cells utilize leukocytes for their extravasation as linkers to the endothelium. Thus, metastasis formation is indirectly susceptible to localization signals that are literally specific for the immune system. We herein compare the extravasation of leukocytes and tumor cells with regard to the involved receptors and the localization signals that direct the cells to certain organs and sites of the body.

[1]  M. Cybulsky,et al.  Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. , 1991, Science.

[2]  W. Muller,et al.  Roles of platelet/endothelial cell adhesion molecule-1 (PECAM-1, CD31) in natural killer cell transendothelial migration and beta 2 integrin activation. , 1996, Journal of immunology.

[3]  Klaus Ley,et al.  CD24 mediates rolling of breast carcinoma cells on P‐selectin , 1998, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[4]  H. Broxmeyer Chemokines in hematopoiesis , 2008, Current opinion in hematology.

[5]  B. Yard,et al.  Modulation of chemokine production and expression of adhesion molecules in renal tubular epithelial and endothelial cells by catecholamines , 2002, Transplantation.

[6]  Alberto Mantovani,et al.  Inflammation and cancer: back to Virchow? , 2001, The Lancet.

[7]  T. Springer,et al.  High endothelial venules (HEVs): specialized endothelium for lymphocyte migration. , 1995, Immunology today.

[8]  F. Luscinskas,et al.  Endothelial-Dependent Mechanisms of Leukocyte Recruitment to the Vascular Wall , 2007, Circulation research.

[9]  R. Lotan,et al.  Expression of galectins on microvessel endothelial cells and their involvement in tumour cell adhesion , 1994, Glycoconjugate Journal.

[10]  V. Kuchroo,et al.  The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity , 2005, Nature Immunology.

[11]  M. Teitell,et al.  An anti-apoptotic role for galectin-3 in diffuse large B-cell lymphomas. , 2004, The American journal of pathology.

[12]  M. Cybulsky,et al.  A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. , 2001, The Journal of clinical investigation.

[13]  R. Sackstein The bone marrow is akin to skin: HCELL and the biology of hematopoietic stem cell homing. , 2004, The journal of investigative dermatology. Symposium proceedings.

[14]  J. Hirabayashi,et al.  A novel biological activity for galectin-1: inhibition of leukocyte-endothelial cell interactions in experimental inflammation. , 2003, The American journal of pathology.

[15]  S. Hwang,et al.  Chemokines, chemokine receptors, and cancer metastasis , 2006, Journal of leukocyte biology.

[16]  P. Altevogt,et al.  The L1 adhesion molecule is a cellular ligand for VLA-5 , 1995, The Journal of cell biology.

[17]  S. Barthel,et al.  Targeting selectins and selectin ligands in inflammation and cancer , 2007, Expert opinion on therapeutic targets.

[18]  N. Chen,et al.  Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the beta-catenin signaling pathway. , 2005, Molecular biology of the cell.

[19]  D. Vestweber Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium , 2007, Immunological reviews.

[20]  Hiroto Kawashima,et al.  Roles of sulfated glycans in lymphocyte homing. , 2006, Biological & pharmaceutical bulletin.

[21]  W. Muller,et al.  CD99 plays a major role in the migration of monocytes through endothelial junctions , 2002, Nature Immunology.

[22]  J. Becker,et al.  Human neural cell adhesion molecule L1 and rat homologue NILE are ligands for integrin alpha v beta 3 , 1996, The Journal of cell biology.

[23]  S. Shimizu,et al.  CX3CR1 is expressed by prostate epithelial cells and androgens regulate the levels of CX3CL1/fractalkine in the bone marrow: potential role in prostate cancer bone tropism. , 2008, Cancer research.

[24]  S. Rosen,et al.  Commentary Endothelial Ligands for L-Selectin From Lymphocyte Recirculation to Allograft Rejection , 1999 .

[25]  B. Imhof,et al.  Vascular and epithelial junctions: a barrier for leucocyte migration. , 2008, Biochemical Society transactions.

[26]  K. Konstantopoulos,et al.  Variant isoforms of CD44 are P‐ and L‐selectin ligands on colon carcinoma cells , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[27]  F. Entschladen,et al.  Surface molecules regulating rolling and adhesion to endothelium of neutrophil granulocytes and MDA-MB-468 breast carcinoma cells and their interaction , 2007, Cellular and Molecular Life Sciences.

[28]  N. Matthews,et al.  Studies of lymphocyte transendothelial migration: analysis of migrated cell phenotypes with regard to CD31 (PECAM-1), CD45RA and CD45RO. , 1993, Immunology.

[29]  W. Hatzmann,et al.  Realtime visualization of tumor cell/endothelial cell interactions during transmigration across the endothelial barrier , 2002, Journal of Cancer Research and Clinical Oncology.

[30]  J. Hirabayashi,et al.  Galectin-3 Interaction with Thomsen-Friedenreich Disaccharide on Cancer-associated MUC1 Causes Increased Cancer Cell Endothelial Adhesion* , 2007, Journal of Biological Chemistry.

[31]  J. Hogg,et al.  Neutrophil kinetics in rabbits during infusion of zymosan-activated plasma. , 1989, Journal of applied physiology.

[32]  A. Griffioen,et al.  Galectins in the tumor endothelium: opportunities for combined cancer therapy. , 2007, Blood.

[33]  J. Hogg,et al.  Marginated pool of neutrophils in rabbit lungs. , 1987, Journal of applied physiology.

[34]  E. Waubant,et al.  T cell gelatinases mediate basement membrane transmigration in vitro. , 1995, Journal of immunology.

[35]  W. Aird Phenotypic Heterogeneity of the Endothelium: II. Representative Vascular Beds , 2007, Circulation research.

[36]  K. Pienta,et al.  Identification of leukocyte E-selectin ligands, P-selectin glycoprotein ligand-1 and E-selectin ligand-1, on human metastatic prostate tumor cells. , 2005, Cancer research.

[37]  A. Montgomery,et al.  Involvement of integrin alpha(v)beta(3) and cell adhesion molecule L1 in transendothelial migration of melanoma cells. , 2001, Molecular biology of the cell.

[38]  D. Vestweber,et al.  A CD99-related antigen on endothelial cells mediates neutrophil but not lymphocyte extravasation in vivo. , 2007, Blood.

[39]  F. Balkwill Cancer and the chemokine network , 2004, Nature Reviews Cancer.

[40]  J. Hogg,et al.  Comparison of neutrophil and capillary diameters and their relation to neutrophil sequestration in the lung. , 1993, Journal of applied physiology.

[41]  H. Chen,et al.  Differential movements of VE-cadherin and PECAM-1 during transmigration of polymorphonuclear leukocytes through human umbilical vein endothelium. , 2002, Blood.

[42]  F. Sarkar,et al.  Galectin-3 and L1 retrotransposons in human breast carcinomas , 1998, Breast Cancer Research and Treatment.

[43]  M. Ghazizadeh,et al.  T/Tn pancarcinoma autoantigens: fundamental, diagnostic, and prognostic aspects. , 1995, Cancer detection and prevention.

[44]  David R. Nadeau,et al.  Heparin and cancer revisited: Mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Fukuda,et al.  Nepmucin, a novel HEV sialomucin, mediates L-selectin–dependent lymphocyte rolling and promotes lymphocyte adhesion under flow , 2006, The Journal of experimental medicine.

[46]  G. Rabinovich Galectin-1 as a potential cancer target , 2005, British Journal of Cancer.

[47]  William C. Aird,et al.  Phenotypic Heterogeneity of the Endothelium: I. Structure, Function, and Mechanisms , 2007, Circulation research.

[48]  S. Cunningham,et al.  Cloning of Human Junctional Adhesion Molecule 3 (JAM3) and Its Identification as the JAM2 Counter-receptor* , 2001, The Journal of Biological Chemistry.

[49]  I. Campbell,et al.  Transmembrane and cytoplasmic domains in integrin activation and protein-protein interactions (Review) , 2008, Molecular membrane biology.

[50]  J. Foidart,et al.  Expression of Lamp‐1 and Lamp‐2 and their interactions with galectin‐3 in human tumor cells , 1998, International journal of cancer.

[51]  E. Butcher,et al.  Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues , 2005, Nature Immunology.

[52]  T. Kinashi,et al.  Intracellular signalling controlling integrin activation in lymphocytes , 2005, Nature Reviews Immunology.

[53]  S. Deutscher,et al.  The role of Thomsen-Friedenreich antigen in adhesion of human breast and prostate cancer cells to the endothelium. , 2001, Cancer research.

[54]  M. Arnaout,et al.  Integrin structure, allostery, and bidirectional signaling. , 2005, Annual review of cell and developmental biology.

[55]  G. Downey,et al.  Neutrophil sequestration and migration in localized pulmonary inflammation. Capillary localization and migration across the interalveolar septum. , 1993, The American review of respiratory disease.

[56]  K. Konstantopoulos,et al.  Selectin Ligand Expression Regulates the Initial Vascular Interactions of Colon Carcinoma Cells , 2006, Journal of Biological Chemistry.

[57]  Carlo Laudanna,et al.  Rapid leukocyte integrin activation by chemokines , 2002, Immunological reviews.

[58]  S Paget,et al.  THE DISTRIBUTION OF SECONDARY GROWTHS IN CANCER OF THE BREAST. , 1889 .

[59]  K. Dib,et al.  BETA 2 integrin signaling in leukocytes. , 2000, Frontiers in bioscience : a journal and virtual library.

[60]  K. Miyake,et al.  Involvement of very late activation antigen 4 (VLA-4) and vascular cell adhesion molecule 1 (VCAM-1) in tumor necrosis factor alpha enhancement of experimental metastasis. , 1994, Cancer research.

[61]  Gabriel A. Rabinovich,et al.  Galectins as modulators of tumour progression , 2005, Nature Reviews Cancer.

[62]  B Dewald,et al.  Human chemokines: an update. , 1997, Annual review of immunology.

[63]  B. Engelhardt,et al.  Mini‐review: Transendothelial migration of leukocytes: through the front door or around the side of the house? , 2004, European journal of immunology.

[64]  S. Deutscher,et al.  Effects of Thomsen-Friedenreich antigen-specific peptide P-30 on beta-galactoside-mediated homotypic aggregation and adhesion to the endothelium of MDA-MB-435 human breast carcinoma cells. , 2000, Cancer research.

[65]  Peter Friedl,et al.  Interstitial leukocyte migration and immune function , 2008, Nature Immunology.

[66]  T. Mcclanahan,et al.  Involvement of chemokine receptors in breast cancer metastasis , 2001, Nature.

[67]  Kerstin Lang,et al.  Tumour-cell migration, invasion, and metastasis: navigation by neurotransmitters. , 2004, The Lancet. Oncology.

[68]  K. Konstantopoulos,et al.  Carcinoembryonic Antigen and CD44 Variant Isoforms Cooperate to Mediate Colon Carcinoma Cell Adhesion to E- and L-selectin in Shear Flow* , 2008, Journal of Biological Chemistry.

[69]  R. Sackstein The bone marrow is akin to skin: HCELL and the biology of hematopoietic stem cell homing. , 2004, The Journal of investigative dermatology.

[70]  A. Varki,et al.  Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium. , 1999, The American journal of pathology.

[71]  V. Castronovo,et al.  Galectin-1 expression in prostate tumor-associated capillary endothelial cells is increased by prostate carcinoma cells and modulates heterotypic cell–cell adhesion , 2004, Angiogenesis.

[72]  C. Carman,et al.  Structural basis of integrin regulation and signaling. , 2007, Annual review of immunology.

[73]  E. Dejana,et al.  Involvement of the very late antigen 4 integrin on melanoma in interleukin 1-augmented experimental metastases. , 1995, Cancer research.

[74]  S. Hemmerich,et al.  Sulfation-dependent recognition of high endothelial venules (HEV)- ligands by L-selectin and MECA 79, and adhesion-blocking monoclonal antibody , 1994, The Journal of experimental medicine.

[75]  M. Perretti,et al.  Inhibitory control of endothelial galectin‐1 on in vitro and in vivo lymphocyte trafficking , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[76]  D. Adams,et al.  Proteoglycans on endothelial cells present adhesion-inducing cytokines to leukocytes. , 1993, Immunology today.

[77]  Kenneth L. van Golen,et al.  Stepping out of the flow: capillary extravasation in cancer metastasis , 2007, Clinical & Experimental Metastasis.

[78]  L. Monteiro,et al.  A theoretical model for estimating the margination constant of leukocytes , 2002, BMC Physiology.

[79]  G. Rådegran,et al.  Alterations in the rheological flow profile in conduit femoral artery during rhythmic thigh muscle contractions in humans. , 2005, The Japanese journal of physiology.

[80]  S. Hemmerich,et al.  Binding of L-selectin to the vascular sialomucin CD34. , 1993, Science.

[81]  A. Varki,et al.  L-selectin facilitation of metastasis involves temporal induction of Fut7-dependent ligands at sites of tumor cell arrest. , 2006, Cancer research.

[82]  M. Cybulsky,et al.  Getting to the site of inflammation: the leukocyte adhesion cascade updated , 2007, Nature Reviews Immunology.

[83]  S. Watson,et al.  An endothelial ligand for L-Selectin is a novel mucin-like molecule , 1992, Cell.

[84]  R. Roth,et al.  Neutrophil migration mechanisms, with an emphasis on the pulmonary vasculature. , 2000, Pharmacological reviews.

[85]  D. Vestweber,et al.  Junctional adhesion molecules (JAMs): more molecules with dual functions? , 2004, Journal of Cell Science.

[86]  A. Zernecke,et al.  JAM-1 is a ligand of the β2 integrin LFA-1 involved in transendothelial migration of leukocytes , 2002, Nature Immunology.

[87]  C. E. van der Schoot,et al.  Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues. , 1996, The American journal of pathology.

[88]  R. Hughes Galectins as modulators of cell adhesion. , 2001, Biochimie.

[89]  M. Philippova,et al.  Structure and Functions of Classical Cadherins , 2001, Biochemistry (Moscow).

[90]  A. Félix,et al.  Simple mucin‐type carbohydrate antigens (T, Tn and sialosyl‐Tn) in mucoepidermoid carcinoma of the salivary glands , 1994, Histopathology.

[91]  T. L. Drell,et al.  The norepinephrine‐driven metastasis development of PC‐3 human prostate cancer cells in BALB/c nude mice is inhibited by β‐blockers , 2006, International journal of cancer.

[92]  James J. Campbell,et al.  Cutting Edge: Chemokine Receptor CCR4 Is Necessary for Antigen-Driven Cutaneous Accumulation of CD4 T Cells under Physiological Conditions1 , 2007, The Journal of Immunology.

[93]  P. Kubes,et al.  Molecular mechanisms of leukocyte recruitment: organ-specific mechanisms of action , 2003, Thrombosis and Haemostasis.

[94]  Gerhard Christofori,et al.  Changing neighbours, changing behaviour: cell adhesion molecule‐mediated signalling during tumour progression , 2003, The EMBO journal.

[95]  Julia T. Chu,et al.  HCELL Is the Major E- and L-selectin Ligand Expressed on LS174T Colon Carcinoma Cells* , 2006, Journal of Biological Chemistry.

[96]  M. Miyasaka,et al.  Lymphocyte trafficking across high endothelial venules: dogmas and enigmas , 2004, Nature Reviews Immunology.

[97]  A. Benner,et al.  Molecular fingerprinting and autocrine growth regulation of endothelial cells in a murine model of hepatocellular carcinoma. , 2006, Cancer research.

[98]  C. Doig,et al.  Functional α4-integrin: A newly identified pathway of neutrophil recruitment in critically ill septic patients , 2001, Nature Medicine.

[99]  G. Rabinovich,et al.  Shedding light on the immunomodulatory properties of galectins: Novel regulators of innate and adaptive immune responses , 2004, Glycoconjugate Journal.

[100]  L. Piccio,et al.  Chemokines trigger immediate beta2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. , 2000, Immunity.

[101]  M. Hirashima,et al.  Human Ecalectin, a Variant of Human Galectin-9, Is a Novel Eosinophil Chemoattractant Produced by T Lymphocytes* , 1998, The Journal of Biological Chemistry.

[102]  E. Dejana,et al.  Junctional Adhesion Molecule, a Novel Member of the Immunoglobulin Superfamily That Distributes at Intercellular Junctions and Modulates Monocyte Transmigration , 1998, The Journal of cell biology.

[103]  B. Petri,et al.  Molecular events during leukocyte diapedesis , 2006, The FEBS journal.

[104]  Cheng Zhu,et al.  A catch to integrin activation , 2007, Nature Immunology.

[105]  Sachiko Sato,et al.  Role of Galectin-3 in Leukocyte Recruitment in a Murine Model of Lung Infection by Streptococcus pneumoniae1 , 2008, The Journal of Immunology.

[106]  W. Muller The role of PECAM‐1 (CD31) in leukocyte emigration: studies in vitro and in vivo , 1995, Journal of leukocyte biology.

[107]  D. Phillips,et al.  PECAM-1 is required for transendothelial migration of leukocytes , 1993, The Journal of experimental medicine.

[108]  C. Qualls,et al.  Cell Adhesion Molecules—Update , 1997, Veterinary pathology.

[109]  N. Dolloff,et al.  CX3CR1-Fractalkine Expression Regulates Cellular Mechanisms Involved in Adhesion, Migration, and Survival of Human Prostate Cancer Cells , 2004, Cancer Research.

[110]  Lu-Gang Yu The oncofetal Thomsen–Friedenreich carbohydrate antigen in cancer progression , 2007, Glycoconjugate Journal.

[111]  F. Entschladen,et al.  The cancer's nervous tooth: Considering the neuronal crosstalk within tumors. , 2008, Seminars in cancer biology.

[112]  J. Van Damme,et al.  The role of CXC chemokines and their receptors in cancer. , 2008, Cancer letters.

[113]  D. Hsu,et al.  Galectin-3 and Galectin-1 Bind Distinct Cell Surface Glycoprotein Receptors to Induce T Cell Death1 , 2006, The Journal of Immunology.

[114]  G. Glinsky,et al.  MDA-MB-435 Human Breast Carcinoma Cell Homo- and Heterotypic Adhesion under Flow Conditions Is Mediated in Part by Thomsen-Friedenreich Antigen-Galectin-3 Interactions* , 2003, The Journal of Biological Chemistry.

[115]  M. Perretti,et al.  Novel insights into the inhibitory effects of Galectin‐1 on neutrophil recruitment under flow , 2008, Journal of leukocyte biology.

[116]  B. Brandt,et al.  3D-extravasation model -- selection of highly motile and metastatic cancer cells. , 2005, Seminars in cancer biology.

[117]  C. Gahmberg,et al.  Specific integrin alpha and beta chain phosphorylations regulate LFA-1 activation through affinity-dependent and-independent mechanisms , 2022 .

[118]  S. Fagerholm,et al.  Specific integrin α and β chain phosphorylations regulate LFA-1 activation through affinity-dependent and -independent mechanisms , 2005, The Journal of cell biology.

[119]  S. Hemmerich,et al.  Induction of PNAd and N-acetylglucosamine 6-O-sulfotransferases 1 and 2 in mouse collagen-induced arthritis , 2006, BMC Immunology.

[120]  F. Luscinskas,et al.  CD99 Is a Key Mediator of the Transendothelial Migration of Neutrophils1 , 2007, The Journal of Immunology.

[121]  A. Luster,et al.  Chemokines--chemotactic cytokines that mediate inflammation. , 1998, The New England journal of medicine.

[122]  T. L. Drell,et al.  Effects of Neurotransmitters on the Chemokinesis and Chemotaxis of MDA-MB-468 Human Breast Carcinoma Cells , 2003, Breast Cancer Research and Treatment.

[123]  A. Al-Mehdi,et al.  Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis , 2000, Nature Medicine.