The connectivity of lymphogenous and hematogenous tumor cell dissemination: Biological insights and clinical implications

Clinical and Experimental Metastasis

Volumn 29, Issue 7, 2012, Pages 737-746

  Sleeman, Jonathan P ^a,b   Cady, Blake ^c   Pantel, Klaus ^d  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c CAMBRIDGE HOSPITAL   (United States)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Circulating tumor cell; Lymph node; Metastasis; Stromal progression

Indexed keywords

RNA; TRASTUZUMAB;

BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER PROGNOSIS; CIRCULATING TUMOR CELL; CIRCULATION; CONFERENCE PAPER; DISTANT METASTASIS; DORMANCY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; HEMATOGENOUS TUMOR CELL DISSEMINATION; HUMAN; HYPOTHESIS; LYMPH NODE METASTASIS; METASTASIS; PRIMARY TUMOR; STROMA CELL; VASCULARIZATION;

HUMANS; LYMPH NODES; LYMPHATIC METASTASIS; LYMPHATIC SYSTEM; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; STROMAL CELLS;

EID: 84868208491     PISSN: 02620898     EISSN: 15737276     Source Type: Journal    
DOI: 10.1007/s10585-012-9489-x     Document Type: Conference Paper

References (79)

1. Sleeman JP, Nazarenko I, Thiele W (2011) Do all roads lead to Rome? Routes to metastasis development. Int J Cancer 128(11):2511-2526. doi:10.1002/ijc.26027
2. Cady B (2007) Regional lymph node metastases; a singular manifestation of the process of clinical metastases in cancer: Contemporary animal research and clinical reports suggest unifying concepts. Ann Surg Oncol 14(6):1790-1800
3. Fisher B, Fisher ER (1966) Transmigration of lymph nodes by tumor cells. Science 152(727):1397-1398
4. Fisher B, Fisher ER (1966) The interrelationship of hematogenous and lymphatic tumor cell dissemination. Surg Gynecol Obstet 122(4):791-798
5. Fisher B, Fisher ER (1970) Significance of the interrelationship of the lymph and blood vascular systems in tumor cell dissemination. Prog Clin Cancer 4:84-96
6. Fisher B, Fisher ER (1967) The organ distribution of disseminated 51 Cr-labeled tumor cells. Cancer Res 27(2):412-420
7. Sleeman J, Schmid A, ThieleW (2009) Tumor lymphatics. Semin Cancer Biol 19(5):285
8. Cochran AJ, Huang RR, Lee J, Itakura E, Leong SP, Essner R (2006) Tumour-induced immune modulation of sentinel lymph nodes. Nat Rev Immunol 6(9):659-670. doi:10.1038/nri1919
9. Madden RE, Gyure L (1968) Translymphnodal passage of tumor cells. Oncology 22(4):281-289
10. Kurokawa Y (1970) Experiments on lymph node metastasis by intralymphatic inoculation of rat ascites tumor cells, with special reference to lodgement, passage, and growth of tumor cells in lymph nodes. Gann 61(5):461-471
11. Hewitt HB, Blake E (1975) Quantitative studies of translymphnodal passage of tumour cells naturally disseminated from a non immunogenic murine squamous carcinoma. Br J Cancer 31(1):25-35
12. Carr J, Carr I, Dreher B, Betts K (1980) Lymphatic metastasis: Invasion of lymphatic vessels and efflux of tumour cells in the afferent popliteal lymph as seen in the Walker rat carcinoma. J Pathol 132(4):287-305. doi:10.1002/path.1711320402
13. Grundmann E, Vollmer E (1985) Early local reaction and lymph node permeation of rat carcinoma HH9-cl 14 cells. An immunohistological approach. Pathol Res Pract 179(3):304-309
14. Leijte JA, van der Ploeg IM, Valdes Olmos RA, Nieweg OE, Horenblas S (2009) Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT. J Nucl Med 50(3):364-367. doi:10.2967/jnumed. 108.059733
15. Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L, Massague J (2009) Tumor self-seeding by circulating cancer cells. Cell 139(7):1315-1326. doi:10.1016/j.cell.2009. 11.025
16. Crile G Jr, Isbister W, Deodhar SD (1971) Demonstration that large metastases in lymph nodes disseminate cancer cells to blood and lungs. Cancer 28(3):657
17. Ward PM, Weiss L (1989) Metachronous seeding of lymph node metastases in rats bearing the MT-100-TC mammary carcinoma: The effect of elective lymph node dissection. Breast Cancer Res Treat 14(3):315-320
18. Sleeman JP (2000) The lymph node as a bridgehead in the metastatic dissemination of tumors. Recent Results Cancer Res 157:55-81
19. Wiley HE, Gonzalez EB, Maki W, Wu MT, Hwang ST (2001) Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J Natl Cancer Inst 93(21):1638-1643
20. Shields JD, Emmett MS, Dunn DB, Joory KD, Sage LM, Rigby H, Mortimer PS, Orlando A, Levick JR, Bates DO (2007) Chemokine-mediated migration of melanoma cells towards lymphatics-a mechanism contributing to metastasis. Oncogene 26(21):2997-3005
21. 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
22. Paget S (1889) The distribution of secondary growths in cancer of the breast. Lancet I:571-573
23. Koch F (1939) Zur Frage der Metastasenbildung bei Impftumoren. Z Krebsforsch 48:495-507
24. Nicolson GL (1988) Organ specificity of tumor metastasis: Role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites. Cancer Metastasis Rev 7(2):143-188
25. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastegui E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824): 50-56
26. Arya M, Patel HR, McGurk C, Tatoud R, Klocker H, Masters J, Williamson M (2004) The importance of the CXCL12-CXCR4 chemokine ligand-receptor interaction in prostate cancer metastasis. J Exp Ther Oncol 4(4):291-303
27. Darash-Yahana M, Pikarsky E, Abramovitch R, Zeira E, Pal B, Karplus R, Beider K, Avniel S, Kasem S, Galun E, Peled A (2004) Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis. Faseb J 18(11):1240-1242. doi:10.1096/fj.03-0935fje
28. Gervasoni JE Jr, Taneja C, Chung MA, Cady B (2000) Biologic and clinical significance of lymphadenectomy. Surg Clin N Am 80(6):1631-1673
29. Veronesi U, Marubini E, Mariani L, Valagussa P, Zucali R (1999) The dissection of internal mammary nodes does not improve the survival of breast cancer patients. 30-year results of a randomised trial. Eur J Cancer 35(9):1320-1325
30. Terrone C, Cracco C, Porpiglia F, Bollito E, Scoffone C, Poggio M, Berruti A, Ragni F, Cossu M, Scarpa RM, Rossetti SR (2006) Reassessing the current TNM lymph node staging for renal cell carcinoma. Eur Urol 49(2):324-331. doi:10.1016/j.eururo.2005. 11.014
31. 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
32. Klein CA, Holzel D (2006) Systemic cancer progression and tumor dormancy: Mathematical models meet single cell genomics. Cell Cycle 5(16):1788-1798
33. Klein CA (2009) Parallel progression of primary tumours and metastases. Nat Rev Cancer 9(4):302-312
34. Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, Winkler F (2010) Real-time imaging reveals the single steps of brain metastasis formation. Nat Med 16(1):116-122
35. Sleeman JP, Christofori G, Fodde R, Collard JG, Berx G, Decraene C, Ruegg C (2012) Concepts of metastasis in flux: The stromal progression model. Semin Cancer Biol. doi:10.1016/ j.semcancer.2012.02.007
36. Uhr JW, Pantel K (2011) Controversies in clinical cancer dormancy. Proc Natl Acad Sci USA 108(30):12396-12400
37. Kauffman HM, McBride MA, Delmonico FL (2000) First report of the united network for organ sharing transplant tumor registry: Donors with a history of cancer. Transplantation 70(12):1747-1751
38. Buell JF, Trofe J, Hanaway MJ, Lo A, Rosengard B, Rilo H, Alloway R, Beebe T, First MR, Woodle ES (2001) Transmission of donor cancer into cardiothoracic transplant recipients. Surgery 130 (4):660-666 (discussion 666-668). doi:10.1067/msy.2001. 117102
39. Naumov GN, MacDonald IC, Weinmeister PM, Kerkvliet N, Nadkarni KV, Wilson SM, Morris VL, Groom AC, Chambers AF (2002) Persistence of solitary mammary carcinoma cells in a secondary site: A possible contributor to dormancy. Cancer Res 62(7):2162-2168
40. MacKie RM, Reid R, Junor B (2003) Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N Engl J Med 348(6):567-568. doi:10.1056/NEJM200302063480620
41. Meng S, Tripathy D, Frenkel EP, Shete S, Naftalis EZ, Huth JF, Beitsch PD, Leitch M, Hoover S, Euhus D, Haley B, Morrison L, Fleming TP, Herlyn D, Terstappen LW, Fehm T, Tucker TF, Lane N, Wang J, Uhr JW (2004) Circulating tumor cells in patients with breast cancer dormancy. Clin Cancer Res 10(24):8152-8162
42. Becker R, Lenter MC, Vollkommer T, Boos AM, Pfaff D, Augustin HG, Christian S (2008) Tumor stroma marker endosialin (Tem1) is a binding partner of metastasis-related protein Mac-2 BP/90 K. Faseb J 22(8):3059-3067
43. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the premetastatic niche. Nature 438(7069):820-827
44. Hiratsuka S, Watanabe A, Aburatani H, Maru Y (2006) Tumourmediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 8(12):1369-1375
45. Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H, Maru Y (2008) The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 10(11):1349-1355
46. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M (2007) VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109(3):1010-1017
47. Jakob C, Aust DE, Liebscher B, Baretton GB, Datta K, Muders MH (2011) Lymphangiogenesis in regional lymph nodes is an independent prognostic marker in rectal cancer patients after neoadjuvant treatment. PLoS ONE 6(11):e27402. doi:10.1371/ journal.pone.0027402
48. Pitchford SC, Furze RC, Jones CP, Wengner AM, Rankin SM (2009) Differential mobilization of subsets of progenitor cells from the bone marrow. Cell Stem Cell 4(1):62-72
49. Cristofanilli M, Braun S (2010) Circulating tumor cells revisited. JAMA 303(11):1092-1093
50. Pantel K, Brakenhoff RH (2004) Dissecting the metastatic cascade. Nat Rev Cancer 4(6):448-456
51. Pantel K, Brakenhoff RH, Brandt B (2008) Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 8:329-340
52. Pantel K, Schlimok G, Kutter D, Schaller G, Genz T, Wiebecke B, Backmann R, Funke I, Riethmuller G (1991) Frequent downregulation of major histocompatibility class I antigen expression on individual micrometastatic carcinoma cells. Cancer Res 51(17):4712-4715
53. Braun S, Pantel K, Muller P, Janni W, Hepp F, Kentenich CR, Gastroph S, Wischnik A, Dimpfl T, Kindermann G, Riethmuller G, Schlimok G (2000) Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N Engl J Med 342(8):525-533
54. Kollermann J, Weikert S, Schostak M, Kempkensteffen C, Kleinschmidt K, Rau T, Pantel K (2008) Prognostic significance of disseminated tumor cells in the bone marrow of prostate cancer patients treated with neoadjuvant hormone treatment. J Clin Oncol 26(30):4928-4933
55. Braun S, Vogl FD, Naume B, Janni W, Osborne MP, Coombes RC, Schlimok G, Diel IJ, Gerber B, Gebauer G, Pierga JY, Marth C, Oruzio D, Wiedswang G, Solomayer EF, Kundt G, Strobl B, Fehm T, Wong GY, Bliss J, Vincent-Salomon A, Pantel K (2005) A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med 353(8):793-802
56. Alix-Panabieres C, Schwarzenbach H, Pantel K (2012) Circulating tumor cells and circulating tumor DNA. Annu Rev Med 63:199-215
57. Xenidis N, Ignatiadis M, Apostolaki S, Perraki M, Kalbakis K, Agelaki S, Stathopoulos EN, Chlouverakis G, Lianidou E, Kakolyris S, Georgoulias V, Mavroudis D (2009) Cytokeratin-19 mRNA-positive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol 27(13):2177-2184
58. Riethdorf S, Fritsche H, Muller V, Rau T, Schindlbeck C, Rack B, Janni W, Coith C, Beck K, Janicke F, Jackson S, Gornet T, Cristofanilli M, Pantel K (2007) Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: A validation study of the cell search system. Clin Cancer Res 13(3):920-928
59. Bednarz N, Eltze E, Semjonow A, Rink M, Andreas A, Mulder L, Hannemann J, Fisch M, Pantel K, Weier HU, Bielawski KP, Brandt B (2010) BRCA1 loss preexisting in small subpopulations of prostate cancer is associated with advanced disease and metastatic spread to lymph nodes and peripheral blood. Clin Cancer Res 16(13):3340-3348
60. Joosse SA, Hannemann J, Spotter J, Bauche A, Andreas A, Muller V, Pantel K (2012) Changes in keratin expression during metastatic progression of breast cancer: Impact on the detection of circulating tumor cells. Clin Cancer Res 18(4):993-1003
61. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW, Hayes DF (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351(8):781-791
62. Cohen SJ, Punt CJ, Iannotti N, Saidman BH, Sabbath KD, Gabrail NY, Picus J, Morse M, Mitchell E, Miller MC, Doyle GV, Tissing H, Terstappen LW, Meropol NJ (2008) Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J Clin Oncol 26(19):3213-3221
63. de Bono JS, Scher HI, Montgomery RB, Parker C, Miller MC, Tissing H, Doyle GV, Terstappen LW, Pienta KJ, Raghavan D (2008) Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin Cancer Res 14(19):6302-6309
64. Krebs MG, Sloane R, Priest L, Lancashire L, Hou JM, Greystoke A, Ward TH, Ferraldeschi R, Hughes A, Clack G, Ranson M, Dive C, Blackhall FH (2011) Evaluation and prognostic significance of circulating tumor cells in patients with non-small-cell lung cancer. J Clin Oncol 29(12):1556-1563
65. Pantel K, Deneve E, Nocca D, Coffy A, Vendrell JP, Maudelonde T, Riethdorf S, Alix-Panabieres C (2012) Circulating epithelial cells in patients with benign colon diseases. Clin Chem. doi: 10.1373/clinchem.2011.175570
66. Riethdorf S, Muller V, Zhang L, Rau T, Loibl S, Komor M, Roller M, Huober J, Fehm T, Schrader I, Hilfrich J, Holms F, Tesch H, Eidtmann H, Untch M, von Minckwitz G, Pantel K (2010) Detection and HER2 expression of circulating tumor cells: Prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res 16(9):2634-2645
67. Smirnov DA, Zweitzig DR, Foulk BW, Miller MC, Doyle GV, Pienta KJ, Meropol NJ, Weiner LM, Cohen SJ, Moreno JG, Connelly MC, Terstappen LW, O'Hara SM (2005) Global gene expression profiling of circulating tumor cells. Cancer Res 65(12):4993-4997
68. Watson MA, Ylagan LR, Trinkaus KM, Gillanders WE, Naughton MJ, Weilbaecher KN, Fleming TP, Aft RL (2007) Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients. Clin Cancer Res 13(17):5001-5009
69. Sieuwerts AM, Kraan J, de Bolt Vries J, van der Spoel P, Mostert B, Martens JW, Gratama JW, Sleijfer S, Foekens JA (2009) Molecular characterization of circulating tumor cells in large quantities of contaminating leukocytes by a multiplex real-time PCR. Breast Cancer Res Treat 118(3):455-468
70. Markou A, Strati A, Malamos N, Georgoulias V, Lianidou ES (2011) Molecular characterization of circulating tumor cells in breast cancer by a liquid bead array hybridization assay. Clin Chem 57(3):421-430
71. Alix-Panabieres C, Vendrell JP, Pelle O, Rebillard X, Riethdorf S, Muller V, Fabbro M, Pantel K (2007) Detection and characterization of putative metastatic precursor cells in cancer patients. Clin Chem 53(3):537-539
72. Alix-Panabieres C, Vendrell JP, Slijper M, Pelle O, Barbotte E, Mercier G, Jacot W, Fabbro M, Pantel K (2009) Full length cytokeratin-19 is released by human tumor cells: A potential role in metastatic progression of breast cancer. Breast Cancer Res 11(3):R39
73. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100(7):3983-3988
74. Bartkowiak K, Effenberger KE, Harder S, Andreas A, Buck F, Peter-Katalinic J, Pantel K, Brandt BH (2010) Discovery of a novel unfolded protein response phenotype of cancer stem/progenitor cells from the bone marrow of breast cancer patients. J Proteome Res 9(6):3158-3168
75. Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J, Kim JK, Patel LR, Ying C, Ziegler AM, Pienta MJ, Song J, Wang J, Loberg RD, Krebsbach PH, Pienta KJ, Taichman RS (2011) Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 121(4):1298-1312
76. Balic M, Lin H, Young L, Hawes D, Giuliano A, McNamara G, Datar RH, Cote RJ (2006) Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 12(19): 5615-5621
77. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7(2): 131-142
78. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S (2009) Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 11(4): R46
79. Baehner FL, Li R, Jenkins T, Hwang J, Kashani-Sabet M, Allen RE, Leong SPL (2012) The impact of primary melanoma thickness and microscopic tumor burden in sentinel lymph nodes on melanoma patient survival. Ann Surg Oncol 19:1034-1042