Home LiteratureArticle Details
PMID: 17200205 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Tumor cell transendothelial passage in the absorbing lymphatic vessel of transgenic adenocarcinoma mouse prostate.

The American journal of pathology ·Vol. 170 ·No. 1 ·2007-01-00 ·Pages 334-46

Azzali G

Abstract

The distribution and fine structure of the tumor-associated absorbing lymphatic vessel in the tumor mass of prostate adenocarcinoma and of seminal vesicle metastasis in transgenic mice was studied for the purpose of understanding the modality of tumor cell transendothelial passage from the extravasal matrix into the lymphatic vessel. In the tumor mass, two main cell populations were identified: stromal tumor cells and the invasive phenotype tumor (IPT) cells, having characteristics such as a highly electron-dense matrix rich in small granules lacking a dense core and massed nuclear chromatin, which is positive to immunostaining with anti-SV40 large T antigen antibody. Based on the ultrastructural pictures of different moments of the IPT cell transendothelial passage by ultrathin serial sections of the tumor-associated absorbing lymphatic vessel, the manner of its transendothelial passage through the intraendothelial channel, without involving intercellular contacts, was demonstrated. The presence of IPT cells in the parenchyma of satellite lymph node highlights its significant role in metastatic diffusion. The intraendothelial channel is the reply to the lack of knowledge regarding the intravasation of the tumor cell into the lymphatic circulation. The lymphatic endothelium would organize this channel on the basis of tumor cell-endothelial cell-extravasal matrix molecular interactions, which are as yet unidentified.

MeSH Terms
Adenocarcinoma/metabolism,pathology Animals Antigens, Polyomavirus Transforming/metabolism Cell Communication Cell Movement Cytoplasmic Granules/pathology Endothelium, Lymphatic/pathology,ultrastructure Lymph Nodes/pathology Lymphatic Metastasis/pathology,ultrastructure Male Mice Mice, Inbred C57BL Mice, Nude Mice, Transgenic Microscopy, Electron Prostatic Neoplasms/metabolism,pathology Seminal Vesicles/pathology Stromal Cells/pathology
Chemicals
Antigens, Polyomavirus Transforming
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Azzali Giacomo
Lymphatology Laboratory, Section of Human Anatomy, Department of Human Anatomy, Pharmacology, and Forensic Medicine, University of Parma, Via Gramsci, 14 (Ospedale Maggiore), 43100, Parma, Italy. giacomo.azzali@unipr.it
References (72)
72 references, click to expand
  1. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice.
    Science. 1997 May 30;276(5317):1423-5 PMID: 9162011
  2. Solid stress inhibits the growth of multicellular tumor spheroids.
    Nat Biotechnol. 1997 Aug;15(8):778-83 PMID: 9255794
  3. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4).
    Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):548-53 PMID: 9435229
  4. A causal role for E-cadherin in the transition from adenoma to carcinoma.
    Nature. 1998 Mar 12;392(6672):190-3 PMID: 9515965
  5. The lymphatic vessels and the so-called "lymphatic stomata" of the diaphragm: a morphologic ultrastructural and three-dimensional study.
    Microvasc Res. 1999 Jan;57(1):30-43 PMID: 9882560
  6. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization.
    J Exp Med. 1999 Feb 1;189(3):451-60 PMID: 9927507
  7. Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium.
    Am J Pathol. 1999 Feb;154(2):385-94 PMID: 10027397
  8. Vascular endothelial growth factor-C expression in human prostatic carcinoma and its relationship to lymph node metastasis.
    Br J Cancer. 1999 Apr;80(1-2):309-13 PMID: 10390013
  9. Histochemical analysis of lymphatic endothelial cells in lymphostasis.
    Microsc Res Tech. 2001 Oct 15;55(2):70-80 PMID: 11596152
  10. Lymphatic mapping and sentinel node lymphadenectomy for cancer: an overview.
    Ann Surg Oncol. 2001 Oct;8(9 Suppl):1S-4S PMID: 11599891
  11. Characterization of indolinones which preferentially inhibit VEGF-C- and VEGF-D-induced activation of VEGFR-3 rather than VEGFR-2.
    Eur J Biochem. 2001 Nov;268(21):5530-40 PMID: 11683876
  12. Molecular pathology of tumor metastasis. I. Predictive pathology.
    Pathol Oncol Res. 2001;7(3):217-30 PMID: 11692150
  13. Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma.
    J Natl Cancer Inst. 2001 Nov 7;93(21):1638-43 PMID: 11698568
  14. The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature.
    Genes Dev. 2002 Apr 1;16(7):773-83 PMID: 11937485
  15. Monoclonal antibody D2-40, a new marker of lymphatic endothelium, reacts with Kaposi's sarcoma and a subset of angiosarcomas.
    Mod Pathol. 2002 Apr;15(4):434-40 PMID: 11950918
  16. Lymphatic metastasis in the absence of functional intratumor lymphatics.
    Science. 2002 Jun 7;296(5574):1883-6 PMID: 11976409
  17. Lymphangiogenesis and cancer metastasis.
    Nat Rev Cancer. 2002 Aug;2(8):573-83 PMID: 12154350
  18. The formation of lymphatic vessels and its importance in the setting of malignancy.
    J Exp Med. 2002 Sep 16;196(6):713-8 PMID: 12235205
  19. Lymphatic vessel activation in cancer.
    Ann N Y Acad Sci. 2002 Dec;979:120-30 PMID: 12543722
  20. Lymphatic vessels in colorectal cancer and their relation with inflammatory infiltrate.
    Dis Colon Rectum. 2003 Jan;46(1):40-7 PMID: 12544520
  21. The lymphatics revisited: new perspectives from the hyaluronan receptor LYVE-1.
    Trends Cardiovasc Med. 2003 Jan;13(1):1-7 PMID: 12554094
  22. Intratumoral lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region.
    Cancer Res. 2003 Apr 15;63(8):1920-6 PMID: 12702584
  23. Tumour-cell invasion and migration: diversity and escape mechanisms.
    Nat Rev Cancer. 2003 May;3(5):362-74 PMID: 12724734
  24. Absence of lymphangiogenesis and intratumoural lymph vessels in human metastatic breast cancer.
    J Pathol. 2003 Jun;200(2):195-206 PMID: 12754740
  25. Angiogenesis, lymphangiogenesis, and melanoma metastasis.
    Oncogene. 2003 May 19;22(20):3172-9 PMID: 12789293
  26. Interleukin-8 secreted by endothelial cells induces chemotaxis of melanoma cells through the chemokine receptor CXCR1.
    FASEB J. 2003 Jul;17(10):1292-4 PMID: 12738812
  27. Insights into the mechanisms of lymph node metastasis.
    Cancer. 2003 Jul 15;98(2):413-23 PMID: 12872364
  28. Intratumoral lymphatics and lymph node metastases in papillary thyroid carcinoma.
    Arch Otolaryngol Head Neck Surg. 2003 Jul;129(7):716-9 PMID: 12874070
  29. Models of metastatic prostate cancer: a transgenic perspective.
    Prostate Cancer Prostatic Dis. 2003;6(3):204-11 PMID: 12970722
  30. Axis of evil: molecular mechanisms of cancer metastasis.
    Oncogene. 2003 Sep 29;22(42):6524-36 PMID: 14528277
  31. Lymphatic endothelium: morphological, molecular and functional properties.
    J Cell Biol. 2003 Oct 27;163(2):209-13 PMID: 14581448
  32. Identification of lymphatic vessels in malignant, adenomatous and normal colonic mucosa using the novel immunostain D2-40.
    Oncol Rep. 2004 Jan;11(1):47-50 PMID: 14654901
  33. Transendothelial transport and migration in vessels of the apparatus lymphaticus periphericus absorbens (ALPA).
    Int Rev Cytol. 2003;230:41-87 PMID: 14692681
  34. Pathology: cancer cells compress intratumour vessels.
    Nature. 2004 Feb 19;427(6976):695 PMID: 14973470
  35. Expression of vascular endothelial growth factor receptor-3 by lymphatic endothelial cells is associated with lymph node metastasis in prostate cancer.
    Clin Cancer Res. 2004 Aug 1;10(15):5137-44 PMID: 15297417
  36. PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis.
    Cancer Cell. 2004 Oct;6(4):333-45 PMID: 15488757
  37. Reverse diapedesis; the mechanism of invasion of lymphatic vessels by neoplastic cells.
    Experientia. 1975 May 15;31(5):590-1 PMID: 1140264
  38. The distribution of endocrine-like cells in the human male and female urethral epithelium.
    Experientia. 1976 Mar 15;32(3):377-8 PMID: 1253918
  39. Lymphatic invasion and metastasis.
    Experientia. 1977 Jul 15;33(7):837-43 PMID: 330195
  40. Invasion and metastasis.
    Can Med Assoc J. 1983 May 15;128(10):1164-7 PMID: 6340812
  41. Lymphatic metastasis.
    Cancer Metastasis Rev. 1983;2(3):307-17 PMID: 6367969
  42. Three-dimensional organization of lymphatics and their relationship to blood vessels in rabbit small intestine. A scanning electron microscopic study of corrosion casts.
    Arch Histol Jpn. 1985 Jul;48(3):255-68 PMID: 4062499
  43. Quantitation of human melanoma, carcinoma and sarcoma tumor cell adhesion to lymphatic endothelium.
    Lymphology. 1990 Mar;23(1):4-14 PMID: 2191172
  44. [Methods of the demonstration of the lymphatic vessels].
    Acta Biomed Ateneo Parmense. 1990;61(1-2):41-56 PMID: 1722066
  45. Prostate cancer in a transgenic mouse.
    Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3439-43 PMID: 7724580
  46. Prox1 function is required for the development of the murine lymphatic system.
    Cell. 1999 Sep 17;98(6):769-78 PMID: 10499794
  47. [The lymphatic vessels of the living animal; observations on the movement of the valves and the contraction of the mesenterial collectors].
    Anat Anz. 1951;97(Suppl.):89-92 PMID: 14915071
  48. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.
    J Cell Biol. 1963 Apr;17:208-12 PMID: 13986422
  49. Lymphangiogenic growth factors as markers of tumor metastasis.
    APMIS. 2004 Jul-Aug;112(7-8):539-49 PMID: 15563315
  50. Molecular insights into prostate cancer progression: the missing link of tumor microenvironment.
    J Urol. 2005 Jan;173(1):10-20 PMID: 15592017
  51. Focus on lymphangiogenesis in tumor metastasis.
    Cancer Cell. 2005 Feb;7(2):121-7 PMID: 15710325
  52. Tumor cells caught in the act of invading: their strategy for enhanced cell motility.
    Trends Cell Biol. 2005 Mar;15(3):138-45 PMID: 15752977
  53. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis.
    J Exp Med. 2005 Apr 4;201(7):1089-99 PMID: 15809353
  54. Immunohistochemical and ultrastructural features of neuroendocrine differentiated carcinomas of the prostate: an immunoelectron microscopic study.
    Ultrastruct Pathol. 2005 Sep-Oct;29(5):367-75 PMID: 16257863
  55. Tumor-secreted vascular endothelial growth factor-C is necessary for prostate cancer lymphangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis.
    Cancer Res. 2005 Nov 1;65(21):9789-98 PMID: 16267000
  56. Interactions between cancer cells and the endothelium in metastasis.
    J Pathol. 2000 Feb;190(3):310-29 PMID: 10685065
  57. Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation.
    Cancer Res. 2000 Aug 15;60(16):4324-7 PMID: 10969769
  58. Active interaction of human A375 melanoma cells with the lymphatics in vivo.
    Histochem Cell Biol. 2000 Nov;114(5):373-85 PMID: 11151407
  59. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis.
    EMBO J. 2001 Feb 15;20(4):672-82 PMID: 11179212
  60. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics.
    Nat Med. 2001 Feb;7(2):186-91 PMID: 11175849
  61. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis.
    Nat Med. 2001 Feb;7(2):192-8 PMID: 11175850
  62. Role of lymphangiogenic factors in tumor metastasis.
    Biochim Biophys Acta. 2004 Mar 4;1654(1):3-12 PMID: 14984763
  63. Lymphangiogenesis and tumour metastasis.
    Novartis Found Symp. 2004;256:112-31; discussion 132-6, 259-69 PMID: 15027486
  64. Tumour-cell migration, invasion, and metastasis: navigation by neurotransmitters.
    Lancet Oncol. 2004 Apr;5(4):254-8 PMID: 15050959
  65. Lymph and blood vessel architecture in benign and malignant prostatic tissue: lack of lymphangiogenesis in prostate carcinoma assessed with novel lymphatic marker lymphatic vessel endothelial hyaluronan receptor (LYVE-1).
    J Urol. 2004 Jul;172(1):103-7 PMID: 15201747
  66. Lymphatic endothelium: an important interactive surface for malignant cells.
    Pulm Pharmacol Ther. 2006;19(1):51-60 PMID: 16286238
  67. 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
  68. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3.
    Nat Med. 2001 Feb;7(2):199-205 PMID: 11175851
  69. Involvement of chemokine receptors in breast cancer metastasis.
    Nature. 2001 Mar 1;410(6824):50-6 PMID: 11242036
  70. LYVE-1, the lymphatic system and tumor lymphangiogenesis.
    Trends Immunol. 2001 Jun;22(6):317-21 PMID: 11377291
  71. Markers for the lymphatic endothelium: in search of the holy grail?
    Microsc Res Tech. 2001 Oct 15;55(2):61-9 PMID: 11596151
  72. Lymphangiogenesis: mechanisms, significance and clinical implications.
    EXS. 1997;79:65-112 PMID: 9002221
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
2007-01-00
Pages
334-46
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1762681
Subset
IM
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