Cancer metastasis through the lymphatic versus blood vessels.
Cancer metastasis
Lymphatic and blood vessels
Journal
Clinical & experimental metastasis
ISSN: 1573-7276
Titre abrégé: Clin Exp Metastasis
Pays: Netherlands
ID NLM: 8409970
Informations de publication
Date de publication:
28 Jun 2024
28 Jun 2024
Historique:
received:
26
01
2024
accepted:
10
04
2024
medline:
28
6
2024
pubmed:
28
6
2024
entrez:
28
6
2024
Statut:
aheadofprint
Résumé
Whether cancer cells metastasize from the primary site to the distant sites via the lymphatic vessels or the blood vessels directly into the circulation is still under intense study. In this review article, we follow the journey of cancer cells metastasizing to the sentinel lymph nodes and beyond to the distant sites. We emphasize cancer heterogeneity and microenvironment as major determinants of cancer metastasis. Multiple molecules have been found to be associated with the complicated process of metastasis. Based on the large sentinel lymph node data, it is reasonable to conclude that cancer cells may metastasize through the blood vessels in some cases but in most cases, they use the sentinel lymph nodes as the major gateway to enter the circulation to distant sites.
Identifiants
pubmed: 38940900
doi: 10.1007/s10585-024-10288-0
pii: 10.1007/s10585-024-10288-0
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. https://doi.org/10.1016/j.cell.2011.02.013
doi: 10.1016/j.cell.2011.02.013
pubmed: 21376230
Steuer CE, Ramalingam SS (2018) Tumor mutation burden: leading immunotherapy to the era of precision medicine? J Clin Oncol 36(7):631–632. https://doi.org/10.1200/JCO.2017.76.8770
doi: 10.1200/JCO.2017.76.8770
pubmed: 29337637
Simpson D, Ferguson R, Martinez CN, Kazlow E, Moran U, Heguy A, Hanniford D, Hernando E, Osman I, Kirchhoff T (2017) Mutation burden as a potential prognostic marker of melanoma progression and survival. American Society of Clinical Oncology
Iacobuzio-Donahue CA (2009) Epigenetic changes in cancer. Annu Rev Pathol 4:229–249
doi: 10.1146/annurev.pathol.3.121806.151442
pubmed: 18840073
Darwin C (1859) On the origin of species by means of natural selection. J. Murray, London
Paget S (1889) The distribution of secondary growths in cancer of the breast. Lancet 133(3421):571–573
doi: 10.1016/S0140-6736(00)49915-0
Paduch R (2016) The role of lymphangiogenesis and angiogenesis in tumor metastasis. Cell Oncol (Dordr) 39(5):397–410. https://doi.org/10.1007/s13402-016-0281-9
doi: 10.1007/s13402-016-0281-9
pubmed: 27126599
Nakamura T, Mizuno S (2010) The discovery of Hepatocyte Growth Factor (HGF) and its significance for cell biology, life sciences and clinical medicine. Proceedings of the Japan Academy, Series B 86 (6):588–610. https://doi.org/10.2183/pjab.86.588
Asellius G (1627) De Lactibus, sive lacteis venis, quarto vasorum mesaraicorum genere, novo invento. ex officina Iohannis Maire, Milan
Virchow R (1860) Cellular pathology as based upon physiological and pathological histology. Trans. 2nd ed. of original by Frank Chance edn., London
Halsted WS (1894) I. The results of Operations for the cure of Cancer of the breast performed at the Johns Hopkins Hospital from June, 1889, to January, 1894. Ann Surg 20(5):497–555. https://doi.org/10.1097/00000658-189407000-00075
doi: 10.1097/00000658-189407000-00075
pubmed: 17860107
pmcid: 1493925
Witte M (2022) Lymphatic Systemonics (Fig. 1). In: Leong SPLSN, Zager JS (eds) Cancer metastasis through the lymphovascular system. Section VI, Witte, MH Springer Nature, Switzerland AG, pp 185–186
RS W, MJ B (2022) Imaging of the lymphatic system with relevance to cancer and cancer metastasis. In: Leong SPLSN, Zager JS (eds) Cancer metastasis through the lymphovascular system. Springer Nature, Switzerland AG, pp 249–260
Schwartz FR, James O, Kuo PH, Witte MH, Koweek LM, Pabon-Ramos WM (2020) Lymphatic imaging: current noninvasive and invasive techniques. Semin Intervent Radiol 37(3):237–249. https://doi.org/10.1055/s-0040-1713441
doi: 10.1055/s-0040-1713441
pubmed: 32773949
pmcid: 7394578
Bowman CA, Witte MH, Witte CL, Way DL, Nagle RB, Copeland JG, Daschbach CC (1984) Cystic hygroma reconsidered: hamartoma or neoplasm? Primary culture of an endothelial cell line from a massive cervicomediastinal hygroma with bony lymphangiomatosis. Lymphology 17(1):15–22
pubmed: 6425572
MH W, DL W, CL W et al (1997) Lymphangiogenisis: mechanisms, significance and clinical implications. In: Goldberg IVRE (ed) Regulation of angiogenesis. Birkhauser, Basel, pp 65–112
Witte MH, Bernas MJ, Martin CP, Witte CL (2001) Lymphangiogenesis and lymphangiodysplasia: from molecular to clinical lymphology. Microsc Res Tech 55(2):122–145. https://doi.org/10.1002/jemt.1163
doi: 10.1002/jemt.1163
pubmed: 11596157
Leong SP, Witte MH (2022) Lymphangiogenesis: Lymphatic System and Lymph nodes; Cancer Lymphangiogenesis and Metastasis. In: Leong SP, Nathanson SD, Zager JS (eds) Cancer Metastasis through the Lymphovascular System. Springer International Publishing, Switzerland AG, pp 209–229. doi: https://doi.org/10.1007/978-3-030-93084-4_21
doi: 10.1007/978-3-030-93084-4_21
Brouillard P, Witte MH, Erickson RP, Damstra RJ, Becker C, Quere I, Vikkula M (2021) Primary lymphoedema. Nat Rev Dis Primers 7(1):77. https://doi.org/10.1038/s41572-021-00309-7
doi: 10.1038/s41572-021-00309-7
pubmed: 34675250
Witte MH, Erickson RP, Luy L, Brouillard P, Vikkula M (2021) Human chromosome map of lymphedema-lymphangiogenesis genes: Template for current and future discovery. Lymphology 54(4):167–169
pubmed: 35073620
Jackson D (2022) Immune cell trafficking in the lymphatics, hyaluronan biology and tumour metastasis. In: Leong SPLSN, Zager JS (eds) Cancer metastasis through the lymphovascular system. Section 22, Jackson, DG (Section Ed). Springer Nature, Switzerland AG, pp 231–238
doi: 10.1007/978-3-030-93084-4_22
Witte MH, Dellinger MT, Papendieck CM, Boccardo F (2012) Overlapping biomarkers, pathways, processes and syndromes in lymphatic development, growth and neoplasia. Clin Exp Metastasis 29(7):707–727. https://doi.org/10.1007/s10585-012-9493-1
doi: 10.1007/s10585-012-9493-1
pubmed: 22798218
Leong SP, Witte M (2011) The pivotal role of the Lymphovascular System in Cancer Metastasis: future perspectives. J Surg Oncol 103(6):639–641. https://doi.org/10.1002/jso.21839
doi: 10.1002/jso.21839
pubmed: 21480259
Dvorak HF, Brown LF, Detmar M, Dvorak AM (1995) Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 146(5):1029–1039
pubmed: 7538264
pmcid: 1869291
Novikov NM, Zolotaryova SY, Gautreau AM, Denisov EV (2021) Mutational drivers of cancer cell migration and invasion. Br J Cancer 124(1):102–114. https://doi.org/10.1038/s41416-020-01149-0
doi: 10.1038/s41416-020-01149-0
pubmed: 33204027
Wai Wong C, Dye DE, Coombe DR (2012) The role of immunoglobulin superfamily cell adhesion molecules in cancer metastasis. International journal of cell biology 2012
Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141(1):52–67. https://doi.org/10.1016/j.cell.2010.03.015
doi: 10.1016/j.cell.2010.03.015
pubmed: 20371345
pmcid: 2862057
Bule P, Aguiar SI, Aires-Da-Silva F, Dias JNR (2021) Chemokine-directed tumor microenvironment modulation in cancer immunotherapy. Int J Mol Sci 22(18). https://doi.org/10.3390/ijms22189804
Niu G, Chen X (2010) Vascular endothelial growth factor as an anti-angiogenic target for cancer therapy. Curr Drug Targets 11(8):1000–1017. https://doi.org/10.2174/138945010791591395
doi: 10.2174/138945010791591395
pubmed: 20426765
pmcid: 3617502
Chiang SP, Cabrera RM, Segall JE (2016) Tumor cell intravasation. Am J Physiol Cell Physiol 311(1):C1–C14. https://doi.org/10.1152/ajpcell.00238.2015
doi: 10.1152/ajpcell.00238.2015
pubmed: 27076614
pmcid: 4967137
Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285(21):1182–1186. https://doi.org/10.1056/NEJM197111182852108
doi: 10.1056/NEJM197111182852108
pubmed: 4938153
Zetter BR (1990) The cellular basis of site-specific tumor metastasis. N Engl J Med 322(9):605–612. https://doi.org/10.1056/NEJM199003013220907
doi: 10.1056/NEJM199003013220907
pubmed: 2406604
Jain RK, Martin JD, Stylianopoulos T (2014) The role of mechanical forces in tumor growth and therapy. Annu Rev Biomed Eng 16:321–346. https://doi.org/10.1146/annurev-bioeng-071813-105259
doi: 10.1146/annurev-bioeng-071813-105259
pubmed: 25014786
pmcid: 4109025
Fares J, Fares MY, Khachfe HH, Salhab HA, Fares Y (2020) Molecular principles of metastasis: a hallmark of cancer revisited. Signal Transduct Target Ther 5(1):28. https://doi.org/10.1038/s41392-020-0134-x
doi: 10.1038/s41392-020-0134-x
pubmed: 32296047
pmcid: 7067809
Leong SP, Naxerova K, Keller L, Pantel K, Witte M (2022) Molecular mechanisms of cancer metastasis via the lymphatic versus the vascular channels. Clin Exp Metas 39(1):159–179. https://doi.org/10.1007/s10585-021-10120-z
doi: 10.1007/s10585-021-10120-z
Ran S, Volk L, Hall K, Flister MJ (2010) Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology 17(4):229–251. https://doi.org/10.1016/j.pathophys.2009.11.003
doi: 10.1016/j.pathophys.2009.11.003
pubmed: 20036110
Hofmann UB, Houben R, Brocker EB, Becker JC (2005) Role of matrix metalloproteinases in melanoma cell invasion. Biochimie 87(3–4):307–314. https://doi.org/10.1016/j.biochi.2005.01.013
doi: 10.1016/j.biochi.2005.01.013
pubmed: 15781317
Barnhill RL, Fandrey K, Levy MA, Mihm MC Jr., Hyman B (1992) Angiogenesis and tumor progression of melanoma. Quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma. Lab Invest 67(3):331–337
pubmed: 1383607
Perivoliotis K, Ntellas P, Dadouli K, Koutoukoglou P, Ioannou M, Tepetes K (2017) Microvessel Density in patients with cutaneous melanoma: an Up-to-date systematic review and Meta-analysis. J Skin Cancer 2017:2049140. https://doi.org/10.1155/2017/2049140
doi: 10.1155/2017/2049140
pubmed: 29441208
pmcid: 5758941
Busam KJ, Berwick M, Blessing K, Fandrey K, Kang S, Karaoli T, Fine J, Cochran AJ, White WL, Rivers J et al (1995) Tumor vascularity is not a prognostic factor for malignant melanoma of the skin. Am J Pathol 147(4):1049–1056
pubmed: 7573350
pmcid: 1871014
Streit M, Detmar M (2003) Angiogenesis, lymphangiogenesis, and melanoma metastasis. Oncogene 22(20):3172–3179. https://doi.org/10.1038/sj.onc.1206457
doi: 10.1038/sj.onc.1206457
pubmed: 12789293
Dadras SS, Paul T, Bertoncini J, Brown LF, Muzikansky A, Jackson DG, Ellwanger U, Garbe C, Mihm MC, Detmar M (2003) Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am J Pathol 162(6):1951–1960. https://doi.org/10.1016/S0002-9440(10)64328-3
doi: 10.1016/S0002-9440(10)64328-3
pubmed: 12759251
pmcid: 1868148
Khare T, Bissonnette M, Khare S (2021) CXCL12-CXCR4/CXCR7 axis in colorectal cancer: therapeutic target in preclinical and clinical studies. Int J Mol Sci 22(14). https://doi.org/10.3390/ijms22147371
Bremnes RM, Camps C, Sirera R (2006) Angiogenesis in non-small cell lung cancer: the prognostic impact of neoangiogenesis and the cytokines VEGF and bFGF in tumours and blood. Lung Cancer 51(2):143–158. https://doi.org/10.1016/j.lungcan.2005.09.005
doi: 10.1016/j.lungcan.2005.09.005
pubmed: 16360975
Zhang X (2019) Interactions between cancer cells and bone microenvironment promote bone metastasis in prostate cancer. Cancer Commun 39(1):76. https://doi.org/10.1186/s40880-019-0425-1
doi: 10.1186/s40880-019-0425-1
Mei S, Chen X, Wang K, Chen Y (2023) Tumor microenvironment in ovarian cancer peritoneal metastasis. Cancer Cell Int 23(1):11. https://doi.org/10.1186/s12935-023-02854-5
doi: 10.1186/s12935-023-02854-5
pubmed: 36698173
pmcid: 9875479
Franchi A, Gallo O, Massi D, Baroni G, Santucci M (2004) Tumor lymphangiogenesis in head and neck squamous cell carcinoma: a morphometric study with clinical correlations. Cancer 101(5):973–978. https://doi.org/10.1002/cncr.20454
doi: 10.1002/cncr.20454
pubmed: 15329906
Cabanas RM (1977) An approach for the treatment of penile carcinoma. Cancer 39(2):456–466. https://doi.org/10.1002/1097-0142(197702)39:2%3C456::aid-cncr2820390214%3E3.0.co;2-i
Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, Foshag LJ, Cochran AJ (1992) Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 127(4):392–399. https://doi.org/10.1001/archsurg.1992.01420040034005
doi: 10.1001/archsurg.1992.01420040034005
pubmed: 1558490
Giuliano AE (2020) The evolution of sentinel node biopsy for breast cancer: personal experience. Breast J 26(1):17–21. https://doi.org/10.1111/tbj.13729
doi: 10.1111/tbj.13729
pubmed: 31876042
Brănişteanu DE, Cozmin M, Porumb-Andrese E, Brănişteanu D, Toader MP, Iosep D, Sinigur D, Brănişteanu CI, Brănişteanu G, Porumb V, Pînzariu AC, Băilă SL, Nicolescu AC (2022) Sentinel Lymph Node Biopsy in Cutaneous Melanoma, a clinical point of View. Medicina 58(11):1589
doi: 10.3390/medicina58111589
pubmed: 36363546
pmcid: 9698247
Hubbard T, Ives C (2020) Significance of a positive sentinel lymph node biopsy in staging for distant metastasis in breast cancer: are current guidelines relevant? Ann R Coll Surg Engl 102(6):429–436. https://doi.org/10.1308/rcsann.2020.0065
doi: 10.1308/rcsann.2020.0065
pubmed: 32326728
pmcid: 7388966
Giuliano AE, Ballman KV, McCall L, Beitsch PD, Brennan MB, Kelemen PR, Ollila DW, Hansen NM, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Morrow M (2017) Effect of Axillary Dissection vs no Axillary dissection on 10-Year overall survival among women with invasive breast Cancer and Sentinel Node Metastasis: the ACOSOG Z0011 (Alliance) Randomized Clinical Trial. JAMA 318(10):918–926. https://doi.org/10.1001/jama.2017.11470
doi: 10.1001/jama.2017.11470
pubmed: 28898379
pmcid: 5672806
Falk Delgado A, Zommorodi S, Falk Delgado A (2019) Sentinel Lymph Node Biopsy and Complete Lymph Node Dissection for Melanoma. Curr Oncol Rep 21(6):54. https://doi.org/10.1007/s11912-019-0798-y
doi: 10.1007/s11912-019-0798-y
pubmed: 31028497
pmcid: 6486528
Che Bakri NA, Kwasnicki RM, Khan N, Ghandour O, Lee A, Grant Y, Dawidziuk A, Darzi A, Ashrafian H, Leff DR (2023) Impact of Axillary Lymph Node Dissection and Sentinel Lymph Node Biopsy on Upper Limb morbidity in breast Cancer patients: a systematic review and Meta-analysis. Ann Surg 277(4):572–580. https://doi.org/10.1097/sla.0000000000005671
doi: 10.1097/sla.0000000000005671
pubmed: 35946806
Cady B (1984) Lymph node metastases. Indicators, but not governors of survival. Arch Surg 119(9):1067–1072. https://doi.org/10.1001/archsurg.1984.01390210063014
doi: 10.1001/archsurg.1984.01390210063014
pubmed: 6383272
Reintgen D, Cruse CW, Wells K, Berman C, Fenske N, Glass F, Schroer K, Heller R, Ross M, Lyman G et al (1994) The orderly progression of melanoma nodal metastases. Ann Surg 220(6):759–767. https://doi.org/10.1097/00000658-199412000-00009
doi: 10.1097/00000658-199412000-00009
pubmed: 7986143
pmcid: 1234478
Leong SP, Pissas A, Scarato M, Gallon F, Pissas MH, Amore M, Wu M, Faries MB, Lund AW (2022) The lymphatic system and sentinel lymph nodes: conduit for cancer metastasis. Clin Exp Metastasis 39(1):139–157. https://doi.org/10.1007/s10585-021-10123-w
doi: 10.1007/s10585-021-10123-w
pubmed: 34651243
Morton DL, Thompson JF, Cochran AJ, Mozzillo N, Elashoff R, Essner R, Nieweg OE, Roses DF, Hoekstra HJ, Karakousis CP (2006) Sentinel-node biopsy or nodal observation in melanoma. N Engl J Med 355(13):1307–1317
doi: 10.1056/NEJMoa060992
pubmed: 17005948
Rios-Cantu A, Lu Y, Melendez-Elizondo V, Chen M, Gutierrez-Range A, Fadaki N, Thummala S, West-Coffee C, Cleaver J, Kashani–Sabet M (2017) Is the non-sentinel lymph node compartment the next site for melanoma progression from the sentinel lymph node compartment in the regional nodal basin? Clin Exp Metastasis 34:345–350
doi: 10.1007/s10585-017-9854-x
pubmed: 28699042
pmcid: 5884118
Andersson Y, Frisell J, Sylvan M, de Boniface J, Bergkvist L (2010) Breast cancer survival in relation to the metastatic tumor burden in axillary lymph nodes. J Clin Oncol 28(17):2868–2873. https://doi.org/10.1200/JCO.2009.24.5001
doi: 10.1200/JCO.2009.24.5001
pubmed: 20458033
Thomas DC, Han G, Leong SP, Kashani-Sabet M, Vetto J, Pockaj B, White RL, Faries MB, Schneebaum S, Mozzillo N (2019) Recurrence of melanoma after a negative sentinel node biopsy: predictors and impact of recurrence site on survival. Ann Surg Oncol 26:2254–2262
doi: 10.1245/s10434-019-07369-w
pubmed: 31011906
Morton DL, Hoon DS, Cochran AJ, Turner RR, Essner R, Takeuchi H, Wanek LA, Glass E, Foshag LJ, Hsueh EC, Bilchik AJ, Elashoff D, Elashoff R (2003) Lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: therapeutic utility and implications of nodal microanatomy and molecular staging for improving the accuracy of detection of nodal micrometastases. Ann Surg 238(4):538–549 Discussion 549–550. https://doi.org/10.1097/01.sla.0000086543.45557.cb
doi: 10.1097/01.sla.0000086543.45557.cb
pubmed: 14530725
pmcid: 1360112
Quiet CA, Ferguson DJ, Weichselbaum RR, Hellman S (1995) Natural history of node-negative breast cancer: a study of 826 patients with long-term follow-up. J Clin Oncol 13(5):1144–1151. https://doi.org/10.1200/JCO.1995.13.5.1144
doi: 10.1200/JCO.1995.13.5.1144
pubmed: 7738620
Saha S, Philimon B, Efeson M, Helina A, Elgamal M, Kiya G, Hilkiah S, Arora M, Wiese D, Kitagawa Y (2022) The role of sentinel lymph node mapping in colon cancer: detection of micro-metastasis, effect on survival, and driver of a paradigm shift in extent of colon resection. Clin Exp Metastasis 39(1):109–115. https://doi.org/10.1007/s10585-021-10121-y
doi: 10.1007/s10585-021-10121-y
pubmed: 34698993
Takeuchi M, Takeuchi H, Kawakubo H, Kitagawa Y (2018) Update on the indications and results of sentinel node mapping in upper GI cancer. Clin Exp Metastasis 35(5):455–461. https://doi.org/10.1007/s10585-018-9934-6
doi: 10.1007/s10585-018-9934-6
pubmed: 30132238
Gershenwald JE, Scolyer RA, Hess KR, Sondak VK, Long GV, Ross MI, Lazar AJ, Faries MB, Kirkwood JM, McArthur GA, Haydu LE, Eggermont AMM, Flaherty KT, Balch CM, Thompson JF, for members of the American Joint Committee on Cancer Melanoma Expert P, the, Melanoma I, Discovery D (2017) P Melanoma staging: Evidence-based changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin 67 (6):472–492. https://doi.org/10.3322/caac.21409
Luke JJ, Rutkowski P, Queirolo P, Del Vecchio M, Mackiewicz J, Chiarion-Sileni V, de la Cruz Merino L, Khattak MA, Schadendorf D, Long GV, Ascierto PA, Mandala M, De Galitiis F, Haydon A, Dummer R, Grob JJ, Robert C, Carlino MS, Mohr P, Poklepovic A, Sondak VK, Scolyer RA, Kirkwood JM, Chen K, Diede SJ, Ahsan S, Ibrahim N, Eggermont AMM, Investigators K- (2022) Pembrolizumab Versus Placebo as Adjuvant Therapy in Resected Stage IIB or IIC Melanoma: Final Analysis of Distant Metastasis-Free Survival in the Phase IIIKEYNOTE-716 Study. J Clin Oncol 42:1619–1624. https://doi.org/10.1200/JCO.23.02355
doi: 10.1016/S0140-6736(22)00562-1
pubmed: 35367007
Fisher B (1980) Laboratory and clinical research in breast cancer–a personal adventure: the David A. Karnofsky memorial lecture. Cancer Res 40(11):3863–3874
pubmed: 7008932
Hellman S, Weichselbaum RR (1995) Oligometastases. J Clin Oncol 13(1):8–10. https://doi.org/10.1200/JCO.1995.13.1.8
doi: 10.1200/JCO.1995.13.1.8
pubmed: 7799047
Pereira ER, Kedrin D, Seano G, Gautier O, Meijer EFJ, Jones D, Chin SM, Kitahara S, Bouta EM, Chang J, Beech E, Jeong HS, Carroll MC, Taghian AG, Padera TP (2018) Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science 359(6382):1403–1407. https://doi.org/10.1126/science.aal3622
doi: 10.1126/science.aal3622
pubmed: 29567713
pmcid: 6002772
Brown M, Assen FP, Leithner A, Abe J, Schachner H, Asfour G, Bago-Horvath Z, Stein JV, Uhrin P, Sixt M, Kerjaschki D (2018) Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science 359(6382):1408–1411. https://doi.org/10.1126/science.aal3662
doi: 10.1126/science.aal3662
pubmed: 29567714
Naxerova K, Reiter JG, Brachtel E, Lennerz JK, van de Wetering M, Rowan A, Cai T, Clevers H, Swanton C, Nowak MA, Elledge SJ, Jain RK (2017) Origins of lymphatic and distant metastases in human colorectal cancer. Science 357(6346):55–60. https://doi.org/10.1126/science.aai8515
doi: 10.1126/science.aai8515
pubmed: 28684519
pmcid: 5536201
Nathanson SD, Krag D, Kuerer HM, Newman LA, Brown M, Kerjaschki D, Pereira ER, Padera TP (2018) Breast cancer metastasis through the lympho-vascular system. Clin Exp Metastasis 35(5–6):443–454. https://doi.org/10.1007/s10585-018-9902-1
doi: 10.1007/s10585-018-9902-1
pubmed: 29796854
Nathanson S, Dieterich L, Zhang X, Chitale D, Pusztai L, Reynaud E, Wu Y-H, Ríos-Hoyo A (2023) Associations amongst genes, molecules, cells, and organs in breast cancer metastasis. Clinical & Experimental Metastasis. https://doi.org/10.1007/s10585-023-10230-w
Zhou H, Lei PJ, Padera TP (2021) Progression of Metastasis through Lymphatic System. Cells 10(3). https://doi.org/10.3390/cells10030627
Detmar M, Hirakawa S (2002) The formation of lymphatic vessels and its importance in the setting of malignancy. J Exp Med 196(6):713–718. https://doi.org/10.1084/jem.20021346
doi: 10.1084/jem.20021346
pubmed: 12235205
pmcid: 2194053
Nagasawa S, Kashima Y, Suzuki A, Suzuki Y (2021) Single-cell and spatial analyses of cancer cells: toward elucidating the molecular mechanisms of clonal evolution and drug resistance acquisition. Inflamm Regen 41(1):22. https://doi.org/10.1186/s41232-021-00170-x
doi: 10.1186/s41232-021-00170-x
pubmed: 34271973
pmcid: 8283950
Park J, Kim J, Lewy T, Rice CM, Elemento O, Rendeiro AF, Mason CE (2022) Spatial omics technologies at multimodal and single cell/subcellular level. Genome Biol 23(1):256. https://doi.org/10.1186/s13059-022-02824-6
doi: 10.1186/s13059-022-02824-6
pubmed: 36514162
pmcid: 9746133
Shayan R, Achen MG, Stacker SA (2006) Lymphatic vessels in cancer metastasis: bridging the gaps. Carcinogenesis 27(9):1729–1738. https://doi.org/10.1093/carcin/bgl031
doi: 10.1093/carcin/bgl031
pubmed: 16597644
Fujimoto N, He Y, D’Addio M, Tacconi C, Detmar M, Dieterich LC (2020) Single-cell mapping reveals new markers and functions of lymphatic endothelial cells in lymph nodes. PLoS Biol 18(4):e3000704. https://doi.org/10.1371/journal.pbio.3000704
doi: 10.1371/journal.pbio.3000704
pubmed: 32251437
pmcid: 7162550
Lucas ED, Tamburini BAJ (2019) Lymph node lymphatic endothelial cell expansion and contraction and the programming of the Immune response. Front Immunol 10:36. https://doi.org/10.3389/fimmu.2019.00036
doi: 10.3389/fimmu.2019.00036
pubmed: 30740101
pmcid: 6357284
Aguado BA, Bushnell GG, Rao SS, Jeruss JS, Shea LD (2017) Engineering the pre-metastatic niche. Nat Biomed Eng 1. https://doi.org/10.1038/s41551-017-0077
Chin AR, Wang SE (2016) Cancer tills the Premetastatic Field: mechanistic basis and clinical implications. Clin Cancer Res 22(15):3725–3733. https://doi.org/10.1158/1078-0432.CCR-16-0028
doi: 10.1158/1078-0432.CCR-16-0028
pubmed: 27252414
pmcid: 4970897
Rinderknecht M, Detmar M (2008) Tumor lymphangiogenesis and melanoma metastasis. J Cell Physiol 216(2):347–354. https://doi.org/10.1002/jcp.21494
doi: 10.1002/jcp.21494
pubmed: 18481261
Han D, Thomas DC, Zager JS, Pockaj B, White RL, Leong SP (2016) Clinical utilities and biological characteristics of melanoma sentinel lymph nodes. World J Clin Oncol 7(2):174–188. https://doi.org/10.5306/wjco.v7.i2.174
doi: 10.5306/wjco.v7.i2.174
pubmed: 27081640
pmcid: 4826963
Miyasaka M, Tanaka T (2004) Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nat Rev Immunol 4(5):360–370. https://doi.org/10.1038/nri1354
doi: 10.1038/nri1354
pubmed: 15122201
Hunter MC, Teijeira A, Halin C (2016) T cell trafficking through lymphatic vessels. Front Immunol 7:613. https://doi.org/10.3389/fimmu.2016.00613
doi: 10.3389/fimmu.2016.00613
pubmed: 28066423
pmcid: 5174098
Jackson DG (2023) Lymphatic trafficking of immune cells and insights for cancer metastasis. Clin Exp Metastasis. https://doi.org/10.1007/s10585-023-10229-3
doi: 10.1007/s10585-023-10229-3
pubmed: 37606814
Eklund L, Bry M, Alitalo K (2013) Mouse models for studying angiogenesis and lymphangiogenesis in cancer. Mol Oncol 7(2):259–282. https://doi.org/10.1016/j.molonc.2013.02.007
doi: 10.1016/j.molonc.2013.02.007
pubmed: 23522958
pmcid: 5528409
He Y, Rajantie I, Pajusola K, Jeltsch M, Holopainen T, Yla-Herttuala S, Harding T, Jooss K, Takahashi T, Alitalo K (2005) Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res 65(11):4739–4746. https://doi.org/10.1158/0008-5472.CAN-04-4576
doi: 10.1158/0008-5472.CAN-04-4576
pubmed: 15930292
Karpanen T, Alitalo K (2001) Lymphatic vessels as targets of tumor therapy? J Exp Med 194(6):F37–F42
doi: 10.1084/jem.194.6.F37
pubmed: 11561002
pmcid: 2195960
Yeung KT, Yang J (2017) Epithelial-mesenchymal transition in tumor metastasis. Mol Oncol 11(1):28–39. https://doi.org/10.1002/1878-0261.12017
doi: 10.1002/1878-0261.12017
pubmed: 28085222
Ribatti D, Tamma R, Annese T (2020) Epithelial-mesenchymal transition in Cancer: a historical overview. Transl Oncol 13(6):100773. https://doi.org/10.1016/j.tranon.2020.100773
doi: 10.1016/j.tranon.2020.100773
pubmed: 32334405
pmcid: 7182759
Dafni H, Israely T, Bhujwalla ZM, Benjamin LE, Neeman M (2002) Overexpression of vascular endothelial growth factor 165 drives peritumor interstitial convection and induces lymphatic drain: magnetic resonance imaging, confocal microscopy, and histological tracking of triple-labeled albumin. Cancer Res 62(22):6731–6739
pubmed: 12438274
Harrell MI, Iritani BM, Ruddell A (2007) Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am J Pathol 170(2):774–786. https://doi.org/10.2353/ajpath.2007.060761
doi: 10.2353/ajpath.2007.060761
pubmed: 17255343
pmcid: 1851877
Shields JD, Fleury ME, Yong C, Tomei AA, Randolph GJ, Swartz MA (2007) Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 11(6):526–538. https://doi.org/10.1016/j.ccr.2007.04.020
doi: 10.1016/j.ccr.2007.04.020
pubmed: 17560334
Shi ZD, Ji XY, Qazi H, Tarbell JM (2009) Interstitial flow promotes vascular fibroblast, myofibroblast, and smooth muscle cell motility in 3-D collagen I via upregulation of MMP-1. Am J Physiol Heart Circ Physiol 297(4):H1225–1234. https://doi.org/10.1152/ajpheart.00369.2009
doi: 10.1152/ajpheart.00369.2009
pubmed: 19465549
pmcid: 2770759
Shi X, Young CD, Zhou H, Wang X (2020) Transforming growth factor-beta signaling in Fibrotic diseases and Cancer-Associated fibroblasts. Biomolecules 10(12). https://doi.org/10.3390/biom10121666
Shieh AC, Rozansky HA, Hinz B, Swartz MA (2011) Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res 71(3):790–800. https://doi.org/10.1158/0008-5472.CAN-10-1513
doi: 10.1158/0008-5472.CAN-10-1513
pubmed: 21245098
Swartz MA, Lund AW (2012) Lymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity. Nat Rev Cancer 12(3):210–219. https://doi.org/10.1038/nrc3186
doi: 10.1038/nrc3186
pubmed: 22362216
Ma Q, Dieterich LC, Ikenberg K, Bachmann SB, Mangana J, Proulx ST, Amann VC, Levesque MP, Dummer R, Baluk P, McDonald DM, Detmar M (2018) Unexpected contribution of lymphatic vessels to promotion of distant metastatic tumor spread. Sci Adv 4(8):eaat4758. https://doi.org/10.1126/sciadv.aat4758
doi: 10.1126/sciadv.aat4758
pubmed: 30101193
pmcid: 6082649
Stacker SA, Williams SP, Karnezis T, Shayan R, Fox SB, Achen MG (2014) Lymphangiogenesis and lymphatic vessel remodelling in cancer. Nat Rev Cancer 14(3):159–172. https://doi.org/10.1038/nrc3677
doi: 10.1038/nrc3677
pubmed: 24561443
Faries MB, Thompson JF, Cochran AJ, Andtbacka RH, Mozzillo N, Zager JS, Jahkola T, Bowles TL, Testori A, Beitsch PD, Hoekstra HJ, Moncrieff M, Ingvar C, Wouters M, Sabel MS, Levine EA, Agnese D, Henderson M, Dummer R, Rossi CR, Neves RI, Trocha SD, Wright F, Byrd DR, Matter M, Hsueh E, MacKenzie-Ross A, Johnson DB, Terheyden P, Berger AC, Huston TL, Wayne JD, Smithers BM, Neuman HB, Schneebaum S, Gershenwald JE, Ariyan CE, Desai DC, Jacobs L, McMasters KM, Gesierich A, Hersey P, Bines SD, Kane JM, Barth RJ, McKinnon G, Farma JM, Schultz E, Vidal-Sicart S, Hoefer RA, Lewis JM, Scheri R, Kelley MC, Nieweg OE, Noyes RD, Hoon DSB, Wang HJ, Elashoff DA, Elashoff RM (2017) Completion dissection or observation for sentinel-node metastasis in melanoma. N Engl J Med 376(23):2211–2222. https://doi.org/10.1056/NEJMoa1613210
doi: 10.1056/NEJMoa1613210
pubmed: 28591523
pmcid: 5548388
Fong Y, Coit DG, Woodruff JM, Brennan MF (1993) Lymph node metastasis from soft tissue sarcoma in adults. Analysis of data from a prospective database of 1772 sarcoma patients. Ann Surg 217(1):72–77. https://doi.org/10.1097/00000658-199301000-00012
doi: 10.1097/00000658-199301000-00012
pubmed: 8424704
pmcid: 1242736
Basile G, Mattei JC, Alshaygy I, Griffin AM, Catton CN, Chung PW, Shultz DB, Razak ARA, Demicco EG, Ferguson PC, Wunder JS (2020) Curability of patients with lymph node metastases from extremity soft-tissue sarcoma. Cancer 126(23):5098–5108. https://doi.org/10.1002/cncr.33189
doi: 10.1002/cncr.33189
pubmed: 32910462
Blazer DG 3rd, Lazar AJ, Xing Y, Askew RL, Feig BW, Pisters PW, Pollock RE, Lev D, Hunt KK, Cormier JN (2009) Clinical outcomes of molecularly confirmed clear cell sarcoma from a single institution and in comparison with data from the Surveillance, Epidemiology, and end results registry. Cancer 115(13):2971–2979. https://doi.org/10.1002/cncr.24322
doi: 10.1002/cncr.24322
pubmed: 19402173
Johannesmeyer D, Smith V, Cole DJ, Esnaola NF, Camp ER (2013) The impact of lymph node disease in extremity soft-tissue sarcomas: a population-based analysis. Am J Surg 206(3):289–295. https://doi.org/10.1016/j.amjsurg.2012.10.043
doi: 10.1016/j.amjsurg.2012.10.043
pubmed: 23806824
Blazer DG 3rd, Sabel MS, Sondak VK (2003) Is there a role for sentinel lymph node biopsy in the management of sarcoma? Surg Oncol 12(3):201–206. https://doi.org/10.1016/s0960-7404(03)00030-6
doi: 10.1016/s0960-7404(03)00030-6
pubmed: 12957624
Tseng W (2022) Biology and Clinical Aspects of Sarcoma Progression, Part XV. In: Leong SP NS, Zager JS (ed) Cancer Metastasis Through the Lymphovascular System. Springer International Publishing, Cham. doi: https://doi.org/10.1007/978-3-030-93084-4_57
Ulvmar MH, Makinen T (2016) Heterogeneity in the lymphatic vascular system and its origin. Cardiovasc Res 111(4):310–321. https://doi.org/10.1093/cvr/cvw175
doi: 10.1093/cvr/cvw175
pubmed: 27357637
pmcid: 4996263
Stahl PL, Salmen F, Vickovic S (2016) Visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 353:78–82. https://doi.org/10.1093/cvr/cvw175
Park J, Kim J, Lewy T (2022) Spatial omics technologies at multimodal and single cell/subcellular level. Genome Biol 23:256.