Home LiteratureArticle Details
PMID: 18595683 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Trans-cellular migration: cell-cell contacts get intimate.

Current opinion in cell biology ·Vol. 20 ·No. 5 ·2008-10-00 ·Pages 533-40

Carman CV, Springer TA

Abstract

Trans-cellular migration, the movement of one cell directly through another, seems an unlikely, counterintuitive, and even bizarre process. Trans-cellular migration has been reported for nearly half a century in leukocyte transendothelial migration in vivo, but is not well enough accepted to widely feature in textbook accounts of diapedesis. Recently, the first in vitro and additional in vivo observations of trans-cellular diapedesis have been reported. Mechanisms by which this occurs are just beginning to be elucidated and point to podosome-like protrusive activities in leukocytes and specific fusogenic functions in endothelial cells. Emerging evidence for a quantitatively significant contribution of trans-cellular migration to leukocyte trafficking in increasingly diverse settings suggests that this phenomenon represents an important and physiologic cell biological process.

MeSH Terms
Animals Cell Adhesion/physiology Cell Membrane/metabolism Cell Movement/physiology Cell Surface Extensions/metabolism,ultrastructure Cytoskeleton/metabolism Endothelial Cells/cytology,physiology Humans Leukocytes/cytology,physiology Membrane Fusion/physiology
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Carman Christopher V
Beth Israel Deaconess Medical Center, Department of Medicine, Harvard Medical School, Boston, MA 02215, USA. ccarman@bidmc.harvard.edu
Springer Timothy A
References (63)
63 references, click to expand
  1. Leukocyte extravasation: chemokine transport and presentation by the endothelium.
    Blood. 2002 Dec 1;100(12):3853-60 PMID: 12433694
  2. T-cell function and migration. Two sides of the same coin.
    N Engl J Med. 2000 Oct 5;343(14):1020-34 PMID: 11018170
  3. Endothelial cells proactively form microvilli-like membrane projections upon intercellular adhesion molecule 1 engagement of leukocyte LFA-1.
    J Immunol. 2003 Dec 1;171(11):6135-44 PMID: 14634129
  4. Electron microscopy of leukocytic margination and emigration in acute inflammation in dog pancreas.
    Am J Pathol. 1961 Aug;39:239-56 PMID: 13785547
  5. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration.
    J Cell Biol. 2007 Sep 24;178(7):1279-93 PMID: 17875742
  6. Electron micrographic observations on the emigration of leucocytes.
    Q J Exp Physiol Cogn Med Sci. 1960 Oct;45:343-8 PMID: 13766495
  7. Endothelial attachment and plasmalemmal apposition in the transcellular movement of intravascular leukemic cells entering the myeloid parenchyma.
    Am J Anat. 1989 Oct;186(2):115-26 PMID: 2816780
  8. Transcellular diapedesis is initiated by invasive podosomes.
    Immunity. 2007 Jun;26(6):784-97 PMID: 17570692
  9. Unique structural features that influence neutrophil emigration into the lung.
    Physiol Rev. 2003 Apr;83(2):309-36 PMID: 12663861
  10. Distribution of actin in migrating leukocytes in vivo.
    Cell Tissue Res. 1984;236(3):517-25 PMID: 6467334
  11. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis.
    Physiol Rev. 2004 Jul;84(3):869-901 PMID: 15269339
  12. The initial lesion in experimental allergic neuritis. A phase and electron microscopic study.
    J Exp Med. 1968 Sep 1;128(3):469-95 PMID: 4875326
  13. Leucocytic emigration from inflamed capillaries.
    Nature. 1960 Dec 31;188:1203 PMID: 13785548
  14. Podosomes: adhesion hot-spots of invasive cells.
    Trends Cell Biol. 2003 Jul;13(7):376-85 PMID: 12837608
  15. Internal structure of the postcapillary high-endothelial venules of rodent lymph nodes and Peyer's patches and the transendothelial lymphocyte passage.
    Am J Anat. 1986 Dec;177(4):481-90 PMID: 3812332
  16. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms.
    Circ Res. 2007 Feb 2;100(2):158-73 PMID: 17272818
  17. Ultrastructural analysis of interleukin-1 beta-induced leukocyte recruitment to the rat retina.
    Invest Ophthalmol Vis Sci. 1997 Jan;38(1):25-35 PMID: 9008627
  18. Lymphocyte migration through the lymphatic sinuses of the chicken's lymph node.
    Poult Sci. 1985 Jan;64(1):159-68 PMID: 3975195
  19. Structural pathways for macromolecular and cellular transport across the blood-brain barrier during inflammatory conditions. Review.
    Histol Histopathol. 2004 Apr;19(2):535-64 PMID: 15024715
  20. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes.
    Exp Cell Res. 1985 Jul;159(1):141-57 PMID: 2411576
  21. Tumor cell transendothelial passage in the absorbing lymphatic vessel of transgenic adenocarcinoma mouse prostate.
    Am J Pathol. 2007 Jan;170(1):334-46 PMID: 17200205
  22. Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes.
    J Cell Biol. 2002 Jun 24;157(7):1233-45 PMID: 12082081
  23. Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis.
    Nature. 2003 Feb 13;421(6924):748-53 PMID: 12610627
  24. Homing to central nervous system vasculature by antigen-specific lymphocytes. II. Lymphocyte/endothelial cell adhesion during the initial stages of autoimmune demyelination.
    Lab Invest. 1990 Oct;63(4):476-89 PMID: 1700193
  25. Stem cell trafficking in tissue development, growth, and disease.
    Cell. 2008 Feb 22;132(4):612-30 PMID: 18295579
  26. Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP.
    J Exp Med. 1998 Mar 16;187(6):903-15 PMID: 9500793
  27. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils.
    J Exp Med. 2006 Jun 12;203(6):1519-32 PMID: 16754715
  28. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing.
    Stem Cells. 2007 Nov;25(11):2739-49 PMID: 17656645
  29. Vimentin function in lymphocyte adhesion and transcellular migration.
    Nat Cell Biol. 2006 Feb;8(2):156-62 PMID: 16429129
  30. Marrow cell egress: specificity of the site of penetration into the sinus.
    Blood. 1978 Nov;52(5):959-68 PMID: 698400
  31. Sites of egress of inflammatory cells and horseradish peroxidase transport across the blood-brain barrier in a murine model of chronic relapsing experimental allergic encephalomyelitis.
    Acta Neuropathol. 1989;78(4):359-71 PMID: 2782047
  32. SOME ELECTRON MICROSCOPIC OBSERVATIONS ON INTERACTIONS BETWEEN LEUKOCYTES, PLATELETS, AND ENDOTHELIAL CELLS IN ACUTE INFLAMMATION.
    Ann N Y Acad Sci. 1964 Aug 27;116:774-88 PMID: 14212852
  33. In vitro studies of human monocyte migration across endothelium in response to leukotriene B4 and f-Met-Leu-Phe.
    Am J Pathol. 1987 Apr;127(1):157-67 PMID: 3031985
  34. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm.
    Cell. 1994 Jan 28;76(2):301-14 PMID: 7507411
  35. Interleukin-1beta reduces transcellular monocyte diapedesis and compromises endothelial adherens junction integrity.
    Microcirculation. 2005 Oct-Nov;12(7):563-79 PMID: 16207629
  36. On the transendothelial passage of tumor cell from extravasal matrix into the lumen of absorbing lymphatic vessel.
    Microvasc Res. 2006 Jul-Sep;72(1-2):74-85 PMID: 16730031
  37. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow.
    Blood. 2005 Jul 15;106(2):584-92 PMID: 15811956
  38. Chemoattractant signals and beta 2 integrin occupancy at apical endothelial contacts combine with shear stress signals to promote transendothelial neutrophil migration.
    J Immunol. 2004 Dec 15;173(12):7282-91 PMID: 15585851
  39. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains.
    Nat Cell Biol. 2006 Feb;8(2):113-23 PMID: 16429128
  40. Nano-surgery at the leukocyte-endothelial docking site.
    Pflugers Arch. 2008 Apr;456(1):71-81 PMID: 18094992
  41. Diapedesis of mononuclear cells across cerebral venules during experimental autoimmune encephalomyelitis leaves tight junctions intact.
    Acta Neuropathol. 2005 Feb;109(2):181-90 PMID: 15549331
  42. Transcytosis: crossing cellular barriers.
    Physiol Rev. 2003 Jul;83(3):871-932 PMID: 12843411
  43. Macrophage migration through the endothelium in the absorbing peripheral lymphatic vessel of the small intestine.
    J Submicrosc Cytol Pathol. 1990 Apr;22(2):273-80 PMID: 2337889
  44. The "mode" of lymphocyte extravasation through HEV of Peyer's patches and its role in normal homing and inflammation.
    Microvasc Res. 2008 Mar;75(2):227-37 PMID: 17980391
  45. Cell migration in tumors.
    Curr Opin Cell Biol. 2005 Oct;17(5):559-64 PMID: 16098726
  46. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds.
    Circ Res. 2007 Feb 2;100(2):174-90 PMID: 17272819
  47. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade.
    J Exp Med. 2006 Nov 27;203(12):2569-75 PMID: 17116736
  48. THE MIGRATION OF LYMPHOCYTES THROUGH THE ENDOTHELIUM OF VENULES IN LYMPH NODES: AN ELECTRON MICROSCOPE STUDY.
    Proc R Soc Lond B Biol Sci. 1964 Jan 14;159:283-90 PMID: 14114164
  49. Leukocyte transendothelial migration: a junctional affair.
    Semin Immunol. 2002 Apr;14(2):105-13 PMID: 11978082
  50. Leukocyte-epithelial interactions.
    Curr Opin Cell Biol. 2003 Oct;15(5):557-64 PMID: 14519390
  51. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response.
    Trends Immunol. 2003 Jun;24(6):327-34 PMID: 12810109
  52. Settings and mechanisms for trans-cellular diapedesis.
    Front Biosci (Landmark Ed). 2009 Jun 01;14:5066-83 PMID: 19482605
  53. Molecules and structures involved in the adhesion of natural killer cells to vascular endothelium.
    J Exp Med. 1991 Feb 1;173(2):439-48 PMID: 1671081
  54. The blood-retinal barrier in experimental autoimmune uveoretinitis. Leukocyte interactions and functional damage.
    Lab Invest. 1994 Jan;70(1):39-52 PMID: 8302017
  55. Ultrastructural studies define soluble macromolecular, particulate, and cellular transendothelial cell pathways in venules, lymphatic vessels, and tumor-associated microvessels in man and animals.
    Microsc Res Tech. 2002 Jun 1;57(5):289-326 PMID: 12112440
  56. Scanning electron microscopic studies on the route of neutrophil extravasation in the mouse after exposure to the chemotactic peptide N-formyl-methionyl-leucyl-phenylalanine (fMLP).
    Arch Histol Cytol. 1999 Aug;62(3):253-60 PMID: 10495880
  57. Induction of transient macroapertures in endothelial cells through RhoA inhibition by Staphylococcus aureus factors.
    J Cell Biol. 2006 Jun 5;173(5):809-19 PMID: 16754962
  58. Extravasation of polymorphonuclear leukocytes from the cerebral microvasculature. Inflammatory response induced by alpha-bungarotoxin.
    Cell Tissue Res. 1985;242(2):399-407 PMID: 4053172
  59. Rho GTPases and the regulation of endothelial permeability.
    Vascul Pharmacol. 2002 Nov;39(4-5):187-99 PMID: 12747959
  60. Locomotion of monocytes on endothelium is a critical step during extravasation.
    Nat Immunol. 2004 Apr;5(4):393-400 PMID: 15021878
  61. An ultrastructural study of in vivo interactions between lymphocytes and endothelial cells in the pathogenesis of the vascular leak syndrome induced by interleukin-2.
    Cancer. 1991 Nov 15;68(10):2169-74 PMID: 1913455
  62. Endothelial domes encapsulate adherent neutrophils and minimize increases in vascular permeability in paracellular and transcellular emigration.
    PLoS One. 2008 Feb 20;3(2):e1649 PMID: 18297135
  63. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them.
    J Cell Biol. 2004 Oct 25;167(2):377-88 PMID: 15504916
Article Info
Journal
Current opinion in cell biology
Abbr.
Curr Opin Cell Biol
ISSN
0955-0674
Published
2008-10-00
Epub
2008-00-01
Pages
533-40
Language
English
Region
England
NLM ID
8913428
PMCID
PMC2811962
Subset
IM
Grants
NCI NIH HHS · R37 CA031798 · United States
NCI NIH HHS · R37 CA031798-29 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com