Skip to main content

Advertisement

SpringerLink
Log in

Biological resonance for cancer metastasis, a new hypothesis based on comparisons between primary cancers and metastases

  • Review Paper
  • Published:
Cancer Microenvironment

Abstract

Many hypotheses have been proposed to try to explain cancer metastasis. However, they seem to be contradictory and have some limitations. Comparisons of primary tumors and matched metastases provide new insight into metastasis. The results show high concordances and minor differences at multiple scales from organic level to molecular level. The concordances reflect the commonality between primary cancer and metastasis, and also mean that metastatic cancer cells derived from primary cancer are quite conservative in distant sites. The differences reflect variation that cancer cells must acquire new traits to adapt to foreign milieu during the course of evolving into a new tumor in second organs. These comparisons also provided new information on understanding mechanism of vascular metastasis, organ-specific metastasis, and tumor dormancy. The collective results suggest a new hypothesis, biological resonance (bio-resonance) model. The hypothesis has two aspects. One is that primary cancer and matched metastasis have a common progenitor. The other is that both ancestors of primary cancer cells and metastatic cancer cells are under similar microenvironments and receive similar or same signals. When their interactions reach a status similar to primary cancer, metastasis will occur. Compared with previous hypotheses, the bio-resonance hypothesis seems to be more applicable for cancer metastasis to explain how, when and where metastasis occurs. Thus, it has important implications for individual prediction, prevention and treatment of cancer metastasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70

    PubMed  CAS  Google Scholar 

  2. Paget S (1989) The distribution of secondary growths in cancer of the breast. Cancer Metastasis Rev 8:98–101

    PubMed  CAS  Google Scholar 

  3. Ewing J (1928) Neoplastic diseases. WB Saunders, Philadelphia

    Google Scholar 

  4. Nowell PC (1976) The clonal evolution of tumor cell populations. Science 194:23–28

    PubMed  CAS  Google Scholar 

  5. Fidler IJ, Kripke ML (1977) Metastasis results from preexisting variant cells within a malignant tumor. Science 197:893–895

    PubMed  CAS  Google Scholar 

  6. Poste G, Fidler IJ (1980) The pathogenesis of cancer metastasis. Nature 283:139–146

    PubMed  CAS  Google Scholar 

  7. Gray JW (2003) Evidence emerges for early metastasis and parallel evolution of primary and metastatic tumors. Cancer Cell 4:4–6

    PubMed  CAS  Google Scholar 

  8. Klein CA (2009) Parallel progression of primary tumours and metastases. Nat Rev Cancer 9:302–312

    PubMed  CAS  Google Scholar 

  9. Pawelek JM, Chakraborty AK (2008) The cancer cell–leukocyte fusion theory of metastasis. Adv Cancer Res 101:397–444

    PubMed  CAS  Google Scholar 

  10. Pawelek JM, Chakraborty AK (2008) Fusion of tumour cells with bone marrow-derived cells: A unifying explanation for metastasis. Nat Rev Cancer 8:377–386

    PubMed  CAS  Google Scholar 

  11. Pawelek, JM (2005) Tumor-cell fusion as a source of myeloid traits in cancer. Lancet Oncol 6:988–993

    Google Scholar 

  12. Li F, Tiede B, Massague J, Kang Y (2007) Beyond tumorigenesis: Cancer stem cells in metastasis. Cell Res 17:3–14

    PubMed  CAS  Google Scholar 

  13. Wicha MS (2006) Cancer stem cells and metastasis: Lethal seeds. Clin Cancer Res 12:5606–5607

    PubMed  Google Scholar 

  14. Korycka BM, Hill RP (1989) Dynamic heterogeneity: Experimental metastasis studies with rif-1 fibrosarcoma. Clin Exp Metastasis 7:107–116

    PubMed  CAS  Google Scholar 

  15. Ling V, Chambers AF, Harris JF, Hill RP (1984) Dynamic heterogeneity and metastasis. J Cell Physiol Suppl 3:99–103

    PubMed  CAS  Google Scholar 

  16. Hill RP, Chambers AF, Ling V, Harris JF (1984) Dynamic heterogeneity: Rapid generation of metastatic variants in mouse b16 melanoma cells. Science 224:998–1001

    PubMed  CAS  Google Scholar 

  17. Bernards R, Weinberg RA (2002) A progression puzzle. Nature 418:823

    PubMed  CAS  Google Scholar 

  18. Weigelt B, Glas AM, Wessels LF, Witteveen AT, Peterse JL, Van’T VL (2003) Gene expression profiles of primary breast tumors maintained in distant metastases. Proc Natl Acad Sci U S A 100:15901–15905

    PubMed  CAS  Google Scholar 

  19. Dong F, Budhu AS, Wang XW (2009) Translating the metastasis paradigm from scientific theory to clinical oncology. Clin Cancer Res 15:2588–2593

    PubMed  Google Scholar 

  20. Talmadge JE, Fidler IJ (2010) AACR centennial series: The biology of cancer metastasis: Historical perspective. Cancer Res 70:5649–5669

    Google Scholar 

  21. Webb T (2003) Microarray studies challenge theories of metastasis. J Natl Cancer Inst : 95:350–351

    Google Scholar 

  22. Dolgin E (2009) Cancer metastasis scrutinized. Nature 461:854–855

    PubMed  CAS  Google Scholar 

  23. Maher EA, Mietz J, Arteaga CL, DePinho RA, Mohla S (2009) Brain metastasis: Opportunities in basic and translational research. Cancer Res 69:6015–6020

    PubMed  CAS  Google Scholar 

  24. Coghlin C, Murray GI (2010) Current and emerging concepts in tumour metastasis. J Pathol 222:1–15

    PubMed  CAS  Google Scholar 

  25. Zajdela A, Asselain B, Ghossein NA (1985) Comparison between the nuclear diameters of primary and metastatic breast cancer cells obtained by cytologic aspiration. Cancer 56:1605–1610

    PubMed  CAS  Google Scholar 

  26. Szentirmay Z, Udvarhelyi N, Besznyak I (1992) Cellular DNA determination and its significance in the identification of tumor recurrences, metastases and second primary tumors. Orv Hetil 133(2015–2016):2021–2023

    Google Scholar 

  27. Jiang JK, Chen YJ, Lin CH, Yu IT, Lin JK (2005) Genetic changes and clonality relationship between primary colorectal cancers and their pulmonary metastases–an analysis by comparative genomic hybridization. Genes Chromosomes Cancer 43:25–36

    PubMed  CAS  Google Scholar 

  28. Bockmuhl U, You X, Pacyna-Gengelbach M, Arps H, Draf W, Petersen I (2004) CGH pattern of esthesioneuroblastoma and their metastases. Brain Pathol 14:158–163

    Google Scholar 

  29. Alcaraz A, Corral JM, Ribal MJ, Mallofre C, Mengual L, Carrio A, Gil-Vernet SJ, Villavicencio H (2004) Fluorescence in situ hybridization analysis of matched primary tumour and lymph-node metastasis of D1(pT2-3pN1M0) prostate cancer. Bju Int 94:407–411

    Google Scholar 

  30. Korn WM, Yasutake T, Kuo WL, Warren RS, Collins C, Tomita M, Gray J, Waldman FM (1999) Chromosome arm 20q gains and other genomic alterations in colorectal cancer metastatic to liver, as analyzed by comparative genomic hybridization and fluorescence in situ hybridization. Genes Chromosomes Cancer 25:82–90

    PubMed  CAS  Google Scholar 

  31. Al-Mulla F, Keith WN, Pickford IR, Going JJ, Birnie GD (1999) Comparative genomic hybridization analysis of primary colorectal carcinomas and their synchronous metastases. Genes Chromosomes Cancer 24:306–314

    PubMed  CAS  Google Scholar 

  32. Danner BC, Gerdes JS, Jung K, Sander B, Enders C, Liersch T, Seipelt R, Gutenberg A, Gunawan B, Schondube FA, Fuzesi L (2011) Comparison of chromosomal aberrations in primary colorectal carcinomas to their pulmonary metastases. Cancer Genet 204:122–128

    PubMed  CAS  Google Scholar 

  33. Bardi G, Parada LA, Bomme L, Pandis N, Johansson B, Willen R, Fenger C, Kronborg O, Mitelman F, Heim S (1997) Cytogenetic findings in metastases from colorectal cancer. Int J Cancer 72:604–607

    PubMed  CAS  Google Scholar 

  34. Hovey RM, Chu L, Balazs M, DeVries S, Moore D, Sauter G, Carroll PR, Waldman FM (1998) Genetic alterations in primary bladder cancers and their metastases. Cancer Res 58:3555–3560

    PubMed  CAS  Google Scholar 

  35. Tarkkanen M, Huuhtanen R, Virolainen M, Wiklund T, Asko-Seljavaara S, Tukiainen E, Lepantalo M, Elomaa I, Knuutila S (1999) Comparison of genetic changes in primary sarcomas and their pulmonary metastases. Genes Chromosomes Cancer 25:323–331

    PubMed  CAS  Google Scholar 

  36. Frankfurt OS, Greco WR, Slocum HK, Arbuck SG, Gamarra M, Pavelic ZP, Rustum YM (1984) Proliferative characteristics of primary and metastatic human solid tumors by dna flow cytometry. Cytometry 5:629–635

    PubMed  CAS  Google Scholar 

  37. Feichter GE, Kaufmann M, Muller A, Haag D, Eckhardt R, Goerttler K (1989) DNA index and cell cycle analysis of primary breast cancer and synchronous axillary lymph node metastases. Breast Cancer Res Treat 13:17–22

    Google Scholar 

  38. Fox MH, Armstrong LW, Withrow SJ, Powers BE, LaRue SM, Straw RC, Gillette EL (1990) Comparison of dna aneuploidy of primary and metastatic spontaneous canine osteosarcomas. Cancer Res 50:6176–6178

    PubMed  CAS  Google Scholar 

  39. Frankfurt OS, Slocum HK, Rustum YM, Arbuck SG, Pavelic ZP, Petrelli N, Huben RP, Pontes EJ, Greco WR (1984) Flow cytometric analysis of DNA aneuploidy in primary and metastatic human solid tumors. Cytometry 5:71–80

    Google Scholar 

  40. Chin JL, Pontes JE, Frankfurt OS (1985) Flow cytometric deoxyribonucleic acid analysis of primary and metastatic human renal cell carcinoma. J Urol 133:582–585

    PubMed  CAS  Google Scholar 

  41. Kusuzaki K, Hashiguchi S, Hirata M, Takeshita H, Murata H, Ashihara T, Hirasawa Y (1999) Response of dna ploidy to chemotherapy in primary and metastatic lesions in human osteosarcomas. Cancer Lett 138:159–165

    PubMed  CAS  Google Scholar 

  42. Flotte TJ, Pastel-Levy C, Graeme-Cook F, Preffer F, Bell DA (1992) DNA flow cytometry of primary tumors and their skin metastases. Correlation of dna histograms. Am J Dermatopathol 14:19–23

    Google Scholar 

  43. Knijn N, Mekenkamp LJ, Klomp M, Vink-Borger ME, Tol J, Teerenstra S, Meijer JW, Tebar M, Riemersma S, van Krieken JH, Punt CJ, Nagtegaal ID (2011) Kras mutation analysis: A comparison between primary tumours and matched liver metastases in 305 colorectal cancer patients. Br J Cancer 104:1020–1026

    PubMed  CAS  Google Scholar 

  44. Mariani P, Lae M, Degeorges A, Cacheux W, Lappartient E, Margogne A, Pierga JY, Girre V, Mignot L, Falcou MC, Salmon RJ, Delattre O, De Cremoux P (2010) Concordant analysis of KRAS status in primary colon carcinoma and matched metastasis. Anticancer Res 30:4229–4235

    Google Scholar 

  45. Italiano A, Hostein I, Soubeyran I, Fabas T, Benchimol D, Evrard S, Gugenheim J, Becouarn Y, Brunet R, Fonck M, Francois E, Saint-Paul MC, Pedeutour F (2010) Kras and braf mutational status in primary colorectal tumors and related metastatic sites: Biological and clinical implications. Ann Surg Oncol 17:1429–1434

    PubMed  Google Scholar 

  46. Marx AH, Tharun L, Muth J, Dancau AM, Simon R, Yekebas E, Kaifi JT, Mirlacher M, Brummendorf TH, Bokemeyer C, Izbicki JR, Sauter G (2009) Her-2 amplification is highly homogenous in gastric cancer. Hum Pathol 40:769–777

    PubMed  CAS  Google Scholar 

  47. Santini D, Loupakis F, Vincenzi B, Floriani I, Stasi I, Canestrari E, Rulli E, Maltese PE, Andreoni F, Masi G, Graziano F, Baldi GG, Salvatore L, Russo A, Perrone G, Tommasino MR, Magnani M, Falcone A, Tonini G, Ruzzo A (2008) High concordance of kras status between primary colorectal tumors and related metastatic sites: implications for clinical practice. Oncologist 13:1270–1275

    PubMed  CAS  Google Scholar 

  48. Li S, Rosell R, Urban A, Font A, Ariza A, Armengol P, Abad A, Navas JJ, Monzo M (1994) K-ras gene point mutation: A stable tumor marker in non-small cell lung carcinoma. Lung Cancer-J Iaslc 11:19–27

    CAS  Google Scholar 

  49. Tjebbes GW, Leppers VSF, Tilanus MG, Hordijk GJ, Slootweg PJ (1999) P53 tumor suppressor gene as a clonal marker in head and neck squamous cell carcinoma: p53 mutations in primary tumor and matched lymph node metastases. Oral Oncol 35:384–389

    PubMed  CAS  Google Scholar 

  50. Peller S, Halevy A, Slutzki S, Kopilova Y, Rotter V (1995) P53 mutations in matched primary and metastatic human tumors. Mol Carcinog 13:166–172

    PubMed  CAS  Google Scholar 

  51. Reichel MB, Ohgaki H, Petersen I, Kleihues P (1994) P53 mutations in primary human lung tumors and their metastases. Mol Carcinog 9:105–109

    PubMed  CAS  Google Scholar 

  52. Durbecq V, Di Leo A, Cardoso F, Rouas G, Leroy JY, Piccart M, Larsimont D (2003) Comparison of topoisomerase-iialpha gene status between primary breast cancer and corresponding distant metastatic sites. Breast Cancer Res Treat 77:199–204

    PubMed  CAS  Google Scholar 

  53. Schlegel U, Rosenfeld MR, Volkenandt M, Rosenblum M, Dalmau J, Furneaux H (1992) P53 gene mutations in primary lung tumors are conserved in brain metastases. J Neurooncol 14:93–100

    PubMed  CAS  Google Scholar 

  54. Turajlic S, Furney SJ, Lambros MB, Mitsopoulos C, Kozarewa I, Geyer FC, Mackay A, Hakas J, Zvelebil M, Lord CJ, Ashworth A, Thomas M, Stamp G, Larkin J, Reis-Filho JS, Marais R (2012) Whole genome sequencing of matched primary and metastatic acral melanomas. Genome Res 22:196–207

    PubMed  CAS  Google Scholar 

  55. Harrell JC, Prat A, Parker JS, Fan C, He X, Carey L, Anders C, Ewend M, Perou CM (2012) Genomic analysis identifies unique signatures predictive of brain, lung, and liver relapse. Breast Cancer Res Treat 132:523–535

    PubMed  CAS  Google Scholar 

  56. Paris PL, Hofer MD, Albo G, Kuefer R, Gschwend JE, Hautmann RE, Fridyland J, Simko J, Carroll PR, Rubin MA, Collins C (2006) Genomic profiling of hormone-naïve lymph node metastases in patients with prostate cancer1. Neoplasia New York Ny 8:1083–1089

    CAS  Google Scholar 

  57. Vasselli JR, Shih JH, Iyengar SR, Maranchie J, Riss J, Worrell R, Torres-Cabala C, Tabios R, Mariotti A, Stearman R, Merino M, Walther MM, Simon R, Klausner RD, Linehan WM (2003) Predicting survival in patients with metastatic kidney cancer by gene-expression profiling in the primary tumor. Proc Natl Acad Sci U S A 100:6958–6963

    PubMed  CAS  Google Scholar 

  58. Wu JM, Fackler MJ, Halushka MK, Molavi DW, Taylor ME, Teo WW, Griffin C, Fetting J, Davidson NE, De Marzo AM, Hicks JL, Chitale D, Ladanyi M, Sukumar S, Argani P (2008) Heterogeneity of breast cancer metastases: Comparison of therapeutic target expression and promoter methylation between primary tumors and their multifocal metastases. Clin Cancer Res 14:1938–1946

    PubMed  CAS  Google Scholar 

  59. Kuramochi H, Hayashi K, Nakajima G, Kamikozuru H, Yamamoto M, Danenberg KD, Danenberg PV (2010) Epidermal growth factor receptor (EGFR) mrna levels and protein expression levels in primary colorectal cancer and corresponding liver metastases. Cancer Chemother Pharmacol 65:825–831

    Google Scholar 

  60. Kobayashi H, Sugihara K, Uetake H, Higuchi T, Yasuno M, Enomoto M, Iida S, Lenz HJ, Danenberg KD, Danenberg PV (2009) Messenger RNA expression of cox-2 and angiogenic factors in primary colorectal cancer and corresponding liver metastasis. Int J Oncol 34:1147–1153

    Google Scholar 

  61. Stickel JS, Weinzierl AO, Hillen N, Drews O, Schuler MM, Hennenlotter J, Wernet D, Muller CA, Stenzl A, Rammensee HG, Stevanovic S (2009) HLA ligand profiles of primary renal cell carcinoma maintained in metastases. Cancer Immunol Immunother 58:1407–1417

    Google Scholar 

  62. Kuramochi H, Hayashi K, Uchida K, Miyakura S, Shimizu D, Vallbohmer D, Park S, Danenberg KD, Takasaki K, Danenberg PV (2006) 5-fluorouracil-related gene expression levels in primary colorectal cancer and corresponding liver metastasis. Int J Cancer 119:522–526

    PubMed  CAS  Google Scholar 

  63. Li J, Gromov P, Gromova I, Moreira JM, Timmermans-Wielenga V, Rank F, Wang K, Li S, Li H, Wiuf C, Yang H, Zhang X, Bolund L, Celis JE (2008) Omics-based profiling of carcinoma of the breast and matched regional lymph node metastasis. Proteomics 8:5038–5052

    PubMed  CAS  Google Scholar 

  64. Bozzetti C, Negri FV, Lagrasta CA, Crafa P, Bassano C, Tamagnini I, Gardini G, Nizzoli R, Leonardi F, Gasparro D, Camisa R, Cavalli S, Silini EM, Ardizzoni A (2011) Comparison of HER2 status in primary and paired metastatic sites of gastric carcinoma. Br J Cancer 104:1372–1376

    Google Scholar 

  65. Azam M, Qureshi A, Mansoor S (2009) Comparison of estrogen receptors, progesterone receptors and HER2/neu expression between primary and metastatic breast carcinoma. J Pak Med Assoc 59:736–740

    Google Scholar 

  66. Bendardaf R, Algars A, Elzagheid A, Korkeila E, Ristamaki R, Lamlum H, Collan Y, Syrjanen K, Pyrhonen S (2006) Comparison of CD44 expression in primary tumours and metastases of colorectal cancer. Oncol Rep 16:741–746

    Google Scholar 

  67. D’Andrea MR, Limiti MR, Bari M, Zambenedetti P, Montagutti A, Ricci F, Pappagallo GL, Sartori D, Vinante O, Mingazzini PL (2007) Correlation between genetic and biological aspects in primary non-metastatic breast cancers and corresponding synchronous axillary lymph node metastasis. Breast Cancer Res Treat 101:279–284

    PubMed  Google Scholar 

  68. Aschele C, Debernardis D, Lonardi S, Bandelloni R, Casazza S, Monfardini S, Gallo L (2004) Deleted in colon cancer protein expression in colorectal cancer metastases: A major predictor of survival in patients with unresectable metastatic disease receiving palliative fluorouracil-based chemotherapy. J Clin Oncol 22:3758–3765

    PubMed  CAS  Google Scholar 

  69. Tsutsui S, Ohno S, Murakami S, Kataoka A, Kinoshita J, Haehitanda Y(2002) EGFR c-erB2 and p53 protein in the primary lesions and paired metastatic regional lymph nodes in breast cancer. Eur J Surg Oncol 28:383–387

    Google Scholar 

  70. Italiano A, Saint-Paul MC, Caroli-Bosc FX, Francois E, Bourgeon A, Benchimol D, Gugenheim J, Michiels JF (2005) Epidermal growth factor receptor (EGFR) status in primary colorectal tumors correlates with egfr expression in related metastatic sites: biological and clinical implications. Ann Oncol 16:1503–1507

    Google Scholar 

  71. Bartkova J, Bartek J, Vojtesek B, Lukas J, Rejthar A, Kovarik J, Millis RR, Lane DP, Barnes DM (1993) Immunochemical analysis of the p53 oncoprotein in matched primary and metastatic human tumours. Eur J Cancer 29A:881–886

    PubMed  CAS  Google Scholar 

  72. Lark AL, Livasy CA, Calvo B, Caskey L, Moore DT, Yang X, Cance WG (2003) Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: immunohistochemistry and real-time pcr analyses. Clin Cancer Res 9:215–222

    PubMed  CAS  Google Scholar 

  73. Rodriguez-Burford C, Chhieng DC, Stockard CR, Kleinberg MJ, Barnes MN, Partridge EE, Weiss HL, Grizzle WE (2003) P53 and erbb-2 are not associated in matched cases of primary and metastatic ovarian carcinomas. Dis Markers 19:11–17

    PubMed  CAS  Google Scholar 

  74. Schmid K, Oehl N, Wrba F, Pirker R, Pirker C, Filipits M (2009) EGFR/KRAS/BRAF mutations in primary lung adenocarcinomas and corresponding locoregional lymph node metastases. Clin Cancer Res 15:4554–4560

    Google Scholar 

  75. Katona TM, Jones TD, Wang M, Eble JN, Billings SD, Cheng L (2007) Genetically heterogeneous and clonally unrelated metastases may arise in patients with cutaneous melanoma. Am J Surg Pathol 31:1029–1037

    PubMed  Google Scholar 

  76. Jones TD, Carr MD, Eble JN, Wang M, Lopez-Beltran A, Cheng L (2005) Clonal origin of lymph node metastases in bladder carcinoma. Cancer 104:1901–1910

    PubMed  Google Scholar 

  77. Weigelt B, Hu Z, He X, Livasy C, Carey LA, Ewend MG, Glas AM, Perou CM, Van’T VL (2005) Molecular portraits and 70-gene prognosis signature are preserved throughout the metastatic process of breast cancer. Cancer Res 65:9155–9158

    PubMed  CAS  Google Scholar 

  78. Inamura K, Shimoji T, Ninomiya H, Hiramatsu M, Okui M, Satoh Y, Okumura S, Nakagawa K, Noda T, Fukayama M, Ishikawa Y (2007) A metastatic signature in entire lung adenocarcinomas irrespective of morphological heterogeneity. Hum Pathol 38:702–709

    PubMed  Google Scholar 

  79. Buyse M, Loi S, Van’T VL, Viale G, Delorenzi M, Glas AM, D’Assignies MS, Bergh J, Lidereau R, Ellis P, Harris A, Bogaerts J, Therasse P, Floore A, Amakrane M, Piette F, Rutgers E, Sotiriou C, Cardoso F, Piccart MJ (2006) Validation and clinical utility of a 70-gene prognostic signature for women with node-negative breast cancer. J Natl Cancer Inst 98:1183–1192

    PubMed  CAS  Google Scholar 

  80. van’t Veer L, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:530–536

    Google Scholar 

  81. van de Vijver MJ, He YD, Van’T VL, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, van der Velde T, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347:1999–2009

    PubMed  Google Scholar 

  82. Adib TR, Henderson S, Perrett C, Hewitt D, Bourmpoulia D, Ledermann J, Boshoff C (2004) Predicting biomarkers for ovarian cancer using gene-expression microarrays. Br J Cancer 90:686–692

    PubMed  CAS  Google Scholar 

  83. Baas JM, Krens LL, Guchelaar HJ, Morreau H, Gelderblom H (2011) Concordance of predictive markers for EGFR inhibitors in primary tumors and metastases in colorectal cancer: a review. Oncologist 16:1239–1249

    Google Scholar 

  84. Leong PP, Rezai B, Koch WM, Reed A, Eisele D, Lee DJ, Sidransky D, Jen J, Westra WH (1998) Distinguishing second primary tumors from lung metastases in patients with head and neck squamous cell carcinoma. J Natl Cancer Inst 90:972–977

    PubMed  CAS  Google Scholar 

  85. Cheung ST, Chen X, Guan XY, Wong SY, Tai LS, Ng IO, So S, Fan ST (2002) Identify metastasis-associated genes in hepatocellular carcinoma through clonality delineation for multinodular tumor. Cancer Res 62:4711–4721

    PubMed  CAS  Google Scholar 

  86. Bahrami S, Cheng L, Wang M, Jones TD, Malone JC, Billings SD (2007) Clonal relationships between epidermotropic metastatic melanomas and their primary lesions: a loss of heterozygosity and x-chromosome inactivation-based analysis. Mod Pathol 20:821–827

    PubMed  CAS  Google Scholar 

  87. Ljungberg B, Stenling R, Roos G (1986) DNA content and prognosis in renal cell carcinoma. A comparison between primary tumors and metastases. Cancer 57:2346–2350

    Google Scholar 

  88. Kim SH, Choi SJ, Cho YB, Kang MW, Lee J, Lee WY, Chun HK, Choi YS, Kim HK, Han J, Kim J (2011) Differential gene expression during colon-to-lung metastasis. Oncol Rep 25:629–636

    PubMed  CAS  Google Scholar 

  89. Joensuu H, Klemi PJ (1988) Comparison of nuclear dna content in primary and metastatic differentiated thyroid carcinoma. Am J Clin Pathol 89:35–40

    PubMed  CAS  Google Scholar 

  90. Bossard C, Kury S, Jamet P, Senellart H, Airaud F, Ramee JF, Bezieau S, Matysiak-Budnik T, Laboisse CL, Mosnier JF (2012) Delineation of the infrequent mosaicism of KRAS mutational status in metastatic colorectal adenocarcinomas. J Clin Pathol 65:466–469

    Google Scholar 

  91. Thongwatchara P, Promwikorn W, Srisomsap C, Chokchaichamnankit D, Boonyaphiphat P, Thongsuksai P (2011) Differential protein expression in primary breast cancer and matched axillary node metastasis. Oncol Rep 26:185–191

    PubMed  CAS  Google Scholar 

  92. Gonzalez-Angulo AM, Ferrer-Lozano J, Stemke-Hale K, Sahin A, Liu S, Barrera JA, Burgues O, Lluch AM, Chen H, Hortobagyi GN, Mills GB, Meric-Bernstam F (2011) PI3K pathway mutations and PTEN levels in primary and metastatic breast cancer. Mol Cancer Ther 10:1093–1101

    Google Scholar 

  93. Mole DJ, O’Neill C, Hamilton P, Olabi B, Robinson V, Williams L, Diamond T, El-Tanani M, Campbell FC (2011) Expression of osteopontin coregulators in primary colorectal cancer and associated liver metastases. Br J Cancer 104:1007–1012

    PubMed  CAS  Google Scholar 

  94. Malek JA, Mery E, Mahmoud YA, Al-Azwani EK, Roger L, Huang R, Jouve E, Lis R, Thiery JP, Querleu D, Rafii A (2011) Copy number variation analysis of matched ovarian primary tumors and peritoneal metastasis. PLoS One 6:e28561

    PubMed  CAS  Google Scholar 

  95. Desouki MM, Liao S, Conroy J, Nowak NJ, Shepherd L, Gaile DP, Geradts J (2011) The genomic relationship between primary breast carcinomas and their nodal metastases. Cancer Invest 29:300–307

    PubMed  CAS  Google Scholar 

  96. Chang YL, Wu CT, Shih JY, Lee YC (2011) Comparison of p53 and epidermal growth factor receptor gene status between primary tumors and lymph node metastases in non-small cell lung cancers. Ann Surg Oncol 18:543–550

    PubMed  Google Scholar 

  97. Yancovitz M, Litterman A, Yoon J, Ng E, Shapiro RL, Berman RS, Pavlick AC, Darvishian F, Christos P, Mazumdar M, Osman I, Polsky D (2012) Intra-and inter-tumor heterogeneity of brafmutations in primary and metastatic melanoma. PLoS One 7:e29336

    PubMed  CAS  Google Scholar 

  98. Swoboda A, Rasin-Streden D, Schanab O, Okamoto I, Pehamberger H, Petzelbauer P, Mikula M (2011) Identification of genetic disparity between primary and metastatic melanoma in human patients. Genes Chromosomes Cancer 50:680–688

    PubMed  CAS  Google Scholar 

  99. Xie HL, Li ZY, Gan RL, Li XJ, Zhang QL, Hui M, Zhou XT (2010) Differential gene and protein expression in primary gastric carcinomas and their lymph node metastases as revealed by combined cdna microarray and tissue microarray analysis. J Dig Dis 11:167–175

    PubMed  CAS  Google Scholar 

  100. Monaco SE, Nikiforova MN, Cieply K, Teot LA, Khalbuss WE, Dacic S (2010) A comparison of EGFR and KRAS status in primary lung carcinoma and matched metastases. Hum Pathol 41:94–102

    Google Scholar 

  101. Wu PF, Kuo KT, Kuo LT, Lin YT, Lee WC, Lu YS, Yang CH, Wu RM, Tu YK, Tasi JC, Tseng HM, Tseng SH, Cheng AL, Lin CH (2010) O(6)-methylguanine-dna methyltransferase expression and prognostic value in brain metastases of lung cancers. Lung Cancer-J Iaslc 68:484–490

    Google Scholar 

  102. Kim JH, Jung EJ, Lee HS, Kim MA, Kim WH (2009) Comparative analysis of dna methylation between primary and metastatic gastric carcinoma. Oncol Rep 21:1251–1259

    PubMed  CAS  Google Scholar 

  103. Raynaud CM, Mercier O, Commo F, Dartevelle P, Gomez-Roca C, de Montpreville V, Sabatier L, Soria JC (2009) Telomere length, telomeric proteins and dna damage repair proteins are differentially expressed between primary lung tumors and their adrenal metastases. Lung Cancer-J Iaslc 65:144–149

    Google Scholar 

  104. Meije CB, Swart GW, Lepoole C, Das PK, Van den Oord JJ (2009) Antigenic profiles of individual-matched pairs of primary and melanoma metastases. Hum Pathol 40:1399–1407

    PubMed  CAS  Google Scholar 

  105. Sun M, Behrens C, Feng L, Ozburn N, Tang X, Yin G, Komaki R, Varella-Garcia M, Hong WK, Aldape KD, Wistuba II (2009) Her family receptor abnormalities in lung cancer brain metastases and corresponding primary tumors. Clin Cancer Res 15:4829–4837

    PubMed  CAS  Google Scholar 

  106. Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, Velculescu VE, Kinzler KW, Vogelstein B, Iacobuzio-Donahue CA (2010) Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467:1114–1117

    PubMed  CAS  Google Scholar 

  107. Loupakis F, Pollina L, Stasi I, Ruzzo A, Scartozzi M, Santini D, Masi G, Graziano F, Cremolini C, Rulli E, Canestrari E, Funel N, Schiavon G, Petrini I, Magnani M, Tonini G, Campani D, Floriani I, Cascinu S, Falcone A (2009) PTEN expression and kras mutations on primary tumors and metastases in the prediction of benefit from cetuximab plus irinotecan for patients with metastatic colorectal cancer. J Clin Oncol 27:2622–2629

    Google Scholar 

  108. Munfus-McCray D, Cui M, Zhang Z, Gabrielson E, Askin F, Li QK (2013) Comparison of EGFR and KRAS mutations in primary and unpaired metastatic lung adenocarcinoma with potential chemotherapy effect. Hum Pathol 44:1286–1292

    Google Scholar 

  109. Gow CH, Chang YL, Hsu YC, Tsai MF, Wu CT, Yu CJ, Yang CH, Lee YC, Yang PC, Shih JY (2009) Comparison of epidermal growth factor receptor mutations between primary and corresponding metastatic tumors in tyrosine kinase inhibitor-naive non-small-cell lung cancer. Ann Oncol 20:696–702

    PubMed  Google Scholar 

  110. Bozzetti C, Tiseo M, Lagrasta C, Nizzoli R, Guazzi A, Leonardi F, Gasparro D, Spiritelli E, Rusca M, Carbognani P, Majori M, Franciosi V, Rindi G, Ardizzoni A (2008) Comparison between epidermal growth factor receptor (egfr) gene expression in primary non-small cell lung cancer (nsclc) and in fine-needle aspirates from distant metastatic sites. J Thorac Oncol 3:18–22

    PubMed  Google Scholar 

  111. Kalikaki A, Koutsopoulos A, Trypaki M, Souglakos J, Stathopoulos E, Georgoulias V, Mavroudis D, Voutsina A (2008) Comparison of egfr and k-ras gene status between primary tumours and corresponding metastases in nsclc. Br J Cancer 99:923–929

    PubMed  CAS  Google Scholar 

  112. Ellsworth RE, Seebach J, Field LA, Heckman C, Kane J, Hooke JA, Love B, Shriver CD (2009) A gene expression signature that defines breast cancer metastases. Clin Exp Metastasis 26:205–213

    PubMed  CAS  Google Scholar 

  113. Stark AM, Hugo HH, Tscheslog H, Mehdorn HM (2007) P53, bcl-2 and bax in non-small cell lung cancer brain metastases: A comparison of real-time RT-PCR, ELISA and immunohistochemical techniques. Neurol Res 29:435–440

    Google Scholar 

  114. Houssami N, Macaskill P, Balleine RL, Bilous M, Pegram MD (2011) Her2 discordance between primary breast cancer and its paired metastasis: tumor biology or test artefact? Insights through meta-analysis. Breast Cancer Res Treat 129:659–674

    PubMed  CAS  Google Scholar 

  115. Stoecklein NH, Klein CA (2010) Genetic disparity between primary tumours, disseminated tumour cells, and manifest metastasis. Int J Cancer 126:589–598

    PubMed  CAS  Google Scholar 

  116. Gupta GP, Massague J (2006) Cancer metastasis: Building a framework. Cell 127:679–695

    PubMed  CAS  Google Scholar 

  117. Witz IP (2008) Tumor-microenvironment interactions: Dangerous liaisons. Adv Cancer Res 100:203–229

    PubMed  CAS  Google Scholar 

  118. Klein-Goldberg A, Maman S, Witz IP (2013) The role played by the microenvironment in site-specific metastasis. Cancer Lett

  119. Witz IP (2009) The tumor microenvironment: the making of a paradigm. Cancer Microenviron 2(Suppl 1):9–17

    PubMed  Google Scholar 

  120. Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9:239–252

    PubMed  CAS  Google Scholar 

  121. Chiang AC, Massague J (2008) Molecular basis of metastasis. N Engl J Med 359:2814–2823

    PubMed  CAS  Google Scholar 

  122. Nguyen DX, Massague J (2007) Genetic determinants of cancer metastasis. Nat Rev Genet 8:341–352

    PubMed  CAS  Google Scholar 

  123. Nguyen DX, Bos PD, Massague J (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9:274–284

    PubMed  CAS  Google Scholar 

  124. Edry BL, Maman S, Sagi-Assif O, Meshel T, Nevo I, Bauerle T, Yron I, Witz IP (2011) Lung-residing metastatic and dormant neuroblastoma cells. Am J Pathol 179:524–536

    Google Scholar 

  125. Talmadge JE (2007) Clonal selection of metastasis within the life history of a tumor. Cancer Res 67:11471–11475

    PubMed  CAS  Google Scholar 

  126. Negrini S, Gorgoulis VG, Halazonetis TD (2010) Genomic instability–an evolving hallmark of cancer. Nat Rev Mol Cell Biol 11:220–228

    PubMed  CAS  Google Scholar 

  127. Kuukasjarvi T, Karhu R, Tanner M, Kahkonen M, Schaffer A, Nupponen N, Pennanen S, Kallioniemi A, Kallioniemi OP, Isola J (1997) Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer. Cancer Res 57:1597–1604

    PubMed  CAS  Google Scholar 

  128. Campbell PJ, Yachida S, Mudie LJ, Stephens PJ, Pleasance ED, Stebbings LA, Morsberger LA, Latimer C, McLaren S, Lin ML, McBride DJ, Varela I, Nik-Zainal SA, Leroy C, Jia M, Menzies A, Butler AP, Teague JW, Griffin CA, Burton J, Swerdlow H, Quail MA, Stratton MR, Iacobuzio-Donahue C, Futreal PA (2010) The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467:1109–1113

    PubMed  CAS  Google Scholar 

  129. Baldus SE, Schaefer KL, Engers R, Hartleb D, Stoecklein NH, Gabbert HE (2010) Prevalence and heterogeneity of KRAS, BRAF, and PI3CA mutations in primary colorectal adenocarcinomas and their corresponding metastases. Clin Cancer Res 16:790–799

    Google Scholar 

  130. Singhi AD, Cimino-Mathews A, Jenkins RB, Lan F, Fink SR, Nassar H, Vang R, Fetting JH, Hicks J, Sukumar S, De Marzo AM, Argani P (2012) Myc gene amplification is often acquired in lethal distant breast cancer metastases of unamplified primary tumors. Mod Pathol 25:378–387

    PubMed  CAS  Google Scholar 

  131. Poplawski AB, Jankowski M, Erickson SW, Diaz DST, Partridge EC, Crasto C, Guo J, Gibson J, Menzel U, Bruder CE, Kaczmarczyk A, Benetkiewicz M, Andersson R, Sandgren J, Zegarska B, Bala D, Srutek E, Allison DB, Piotrowski A, Zegarski W, Dumanski JP (2010) Frequent genetic differences between matched primary and metastatic breast cancer provide an approach to identification of biomarkers for disease progression. Eur J Hum Genet 18:560–568

    PubMed  CAS  Google Scholar 

  132. Ganepola GA, Mazziotta RM, Weeresinghe D, Corner GA, Parish CJ, Chang DH, Tebbutt NC, Murone C, Ahmed N, Augenlicht LH, Mariadason JM (2010) Gene expression profiling of primary and metastatic colon cancers identifies a reduced proliferative rate in metastatic tumors. Clin Exp Metastasis 27:1–9

    PubMed  CAS  Google Scholar 

  133. Koda M, Sulkowska M, Kanczuga-Koda L, Sulkowski S (2005) Expression of insulin receptor substrate 1 in primary breast cancer and lymph node metastases. J Clin Pathol 58:645–649

    PubMed  CAS  Google Scholar 

  134. Cavalli LR, Urban CA, Dai D, de Assis S, Tavares DC, Rone JD, Bleggi-Torres LF, Lima RS, Cavalli IJ, Issa JP, Haddad BR (2003) Genetic and epigenetic alterations in sentinel lymph nodes metastatic lesions compared to their corresponding primary breast tumors. Cancer Genet Cytogenet 146:33–40

    PubMed  CAS  Google Scholar 

  135. Hoang CD, Guillaume TJ, Engel SC, Tawfic SH, Kratzke RA, Maddaus MA (2005) Analysis of paired primary lung and lymph node tumor cells: A model of metastatic potential by multiple genetic programs. Cancer Detect Prev 29:509–517

    PubMed  CAS  Google Scholar 

  136. Montel V, Huang TY, Mose E, Pestonjamasp K, Tarin D (2005) Expression profiling of primary tumors and matched lymphatic and lung metastases in a xenogeneic breast cancer model. Am J Pathol 166:1565–1579

    PubMed  CAS  Google Scholar 

  137. Thompson AM, Jordan LB, Quinlan P, Anderson E, Skene A, Dewar JA, Purdie CA (2010) Prospective comparison of switches in biomarker status between primary and recurrent breast cancer: the breast recurrence in tissues study (brits). Breast Cancer Res 12:R92

    PubMed  Google Scholar 

  138. Aitken SJ, Thomas JS, Langdon SP, Harrison DJ, Faratian D (2010) Quantitative analysis of changes in er, pr and her2 expression in primary breast cancer and paired nodal metastases. Ann Oncol 21:1254–1261

    PubMed  CAS  Google Scholar 

  139. Ki DH, Jeung HC, Park CH, Kang SH, Lee GY, Lee WS, Kim NK, Chung HC, Rha SY (2007) Whole genome analysis for liver metastasis gene signatures in colorectal cancer. Int J Cancer 121:2005–2012

    PubMed  CAS  Google Scholar 

  140. Mulder TP, Roelofs HM, Peters WH, Wagenmans MJ, Sier CF, Verspaget HW (1994) Glutathione s-transferases in liver metastases of colorectal cancer. A comparison with normal liver and primary carcinomas. Carcinogenesis 15:2149–2153

    PubMed  CAS  Google Scholar 

  141. Luebeck EG (2010) Cancer: genomic evolution of metastasis. Nature 467:1053–1055

    PubMed  CAS  Google Scholar 

  142. Ding L, Ellis MJ, Li S, Larson DE, Chen K, Wallis JW, Harris CC, McLellan MD, Fulton RS, Fulton LL, Abbott RM, Hoog J, Dooling DJ, Koboldt DC, Schmidt H, Kalicki J, Zhang Q, Chen L, Lin L, Wendl MC, McMichael JF, Magrini VJ, Cook L, McGrath SD, Vickery TL, Appelbaum E, Deschryver K, Davies S, Guintoli T, Lin L, Crowder R, Tao Y, Snider JE, Smith SM, Dukes AF, Sanderson GE, Pohl CS, Delehaunty KD, Fronick CC, Pape KA, Reed JS, Robinson JS, Hodges JS, Schierding W, Dees ND, Shen D, Locke DP, Wiechert ME, Eldred JM, Peck JB, Oberkfell BJ, Lolofie JT, Du F, Hawkins AE, O’Laughlin MD, Bernard KE, Cunningham M, Elliott G, Mason MD, Thompson DJ, Ivanovich JL, Goodfellow PJ, Perou CM, Weinstock GM, Aft R, Watson M, Ley TJ, Wilson RK, Mardis ER (2010) Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 464:999–1005

    PubMed  CAS  Google Scholar 

  143. Alonso GM, Alvarez MC, Llorente JL, Sampedro NA, Suarez C, Hermsen M (2009) Genetic differences between primary larynx and pharynx carcinomas and their matched lymph node metastases by multiplex ligation-dependent probe amplification. Oral Oncol 45:600–604

    Google Scholar 

  144. Suzuki M, Tarin D (2007) Gene expression profiling of human lymph node metastases and matched primary breast carcinomas: clinical implications. Mol Oncol 1:172–180

    PubMed  Google Scholar 

  145. Baba H, Korenaga D, Okamura T, Sugimachi K (1990) Comparison of dna content in gastric cancer cells between primary lesions and lymph node metastases. Cancer 66:1775–1780

    PubMed  CAS  Google Scholar 

  146. Blaker H, Graf M, Rieker RJ, Otto HF (1999) Comparison of losses of heterozygosity and replication errors in primary colorectal carcinomas and corresponding liver metastases. J Pathol 188:258–262

    PubMed  CAS  Google Scholar 

  147. Zhang SY, Bauer B, Mitsunaga S, Goodrow TL, Klein-Szanto AJ (1995) Lack of concordant p53 mutations in some paired primary and metastatic mouse squamous cell carcinomas induced by chemical carcinogenesis. Mol Carcinog 12:77–81

    PubMed  CAS  Google Scholar 

  148. Kropveld A, van Mansfeld AD, Nabben N, Hordijk GJ, Slootweg PJ (1996) Discordance of p53 status in matched primary tumours and metastases in head and neck squamous cell carcinoma patients. Eur J Cancer B Oral Oncol 32B:388–393

    PubMed  CAS  Google Scholar 

  149. Wong SY, Hynes RO (2006) Lymphatic or hematogenous dissemination: How does a metastatic tumor cell decide? Cell Cycle 5:812–817

    PubMed  CAS  Google Scholar 

  150. Tabor MP, van Houten VM, Kummer JA, Vosjan MJ, Vlasblom R, Snow GB, Leemans CR, Braakhuis BJ, Brakenhoff RH (2002) Discordance of genetic alterations between primary head and neck tumors and corresponding metastases associated with mutational status of the TP53 gene. Genes Chromosomes Cancer 33:168–177

    Google Scholar 

  151. Gershenwald JE, Fidler IJ (2002) Cancer. Targeting lymphatic metastasis. Science 296:1811–1812

    PubMed  CAS  Google Scholar 

  152. Pantel K, Brakenhoff RH (2004) Dissecting the metastatic cascade. Nat Rev Cancer 4:448–456

    PubMed  CAS  Google Scholar 

  153. Knosel T, Schluns K, Stein U, Schwabe H, Schlag PM, Dietel M, Petersen I (2004) Chromosomal alterations during lymphatic and liver metastasis formation of colorectal cancer. Neoplasia 6:23–28

    PubMed  Google Scholar 

  154. Ayhan A, Yasui W, Yokozaki H, Kitadai Y, Tahara E (1993) Reduced expression of nm23 protein is associated with advanced tumor stage and distant metastases in human colorectal carcinomas. Virchows Arch B Cell Pathol Incl Mol Pathol 63:213–218

    PubMed  CAS  Google Scholar 

  155. Tie J, Lipton L, Desai J, Gibbs P, Jorissen RN, Christie M, Drummond KJ, Thomson BN, Usatoff V, Evans PM, Pick AW, Knight S, Carne PW, Berry R, Polglase A, McMurrick P, Zhao Q, Busam D, Strausberg RL, Domingo E, Tomlinson IP, Midgley R, Kerr D, Sieber OM (2011) Kras mutation is associated with lung metastasis in patients with curatively resected colorectal cancer. Clin Cancer Res 17:1122–1130

    PubMed  CAS  Google Scholar 

  156. Knosel T, Schluns K, Dietel M, Petersen I (2005) Chromosomal alterations in lung metastases of colorectal carcinomas: associations with tissue specific tumor dissemination. Clin Exp Metastasis 22:533–538

    PubMed  Google Scholar 

  157. Landemaine T, Jackson A, Bellahcene A, Rucci N, Sin S, Abad BM, Sierra A, Boudinet A, Guinebretiere JM, Ricevuto E, Nogues C, Briffod M, Bieche I, Cherel P, Garcia T, Castronovo V, Teti A, Lidereau R, Driouch K (2008) A six-gene signature predicting breast cancer lung metastasis. Cancer Res 68:6092–6099

    PubMed  CAS  Google Scholar 

  158. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3:537–549

    PubMed  CAS  Google Scholar 

  159. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, Minn AJ, van de Vijver MJ, Gerald WL, Foekens JA, Massague J (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459:1005–1009

    PubMed  CAS  Google Scholar 

  160. Maman S, Edry-Botzer L, Sagi-Assif O, Meshel T, Yuan W, Lu W, Witz IP (2013) The metastatic microenvironment: Lung-derived factors control the viability of Neuroblastoma lung metastasis. Int J Cancer 133:2296–2306

    PubMed  CAS  Google Scholar 

  161. Izraely S, Sagi-Assif O, Klein A, Meshel T, Tsarfaty G, Pasmanik-Chor M, Nahmias C, Couraud PO, Ateh E, Bryant JL, Hoon DS, Witz IP (2012) The metastatic microenvironment: Brain-residing melanoma metastasis and dormant micrometastasis. Int J Cancer 131:1071–1082

    PubMed  CAS  Google Scholar 

  162. Alix-Panabieres C, Riethdorf S, Pantel K (2008) Circulating tumor cells and bone marrow micrometastasis. Clin Cancer Res 14:5013–5021

    PubMed  CAS  Google Scholar 

  163. Somlo G, Lau SK, Frankel P, Hsieh HB, Liu X, Yang L, Krivacic R, Bruce RH (2011) Multiple biomarker expression on circulating tumor cells in comparison to tumor tissues from primary and metastatic sites in patients with locally advanced/inflammatory, and stage iv breast cancer, using a novel detection technology. Breast Cancer Res Treat 128:155–163

    PubMed  CAS  Google Scholar 

  164. Khan ZA, Jonas SK, Le-Marer N, Patel H, Wharton RQ, Tarragona A, Ivison A, Allen-Mersh TG (2000) P53 mutations in primary and metastatic tumors and circulating tumor cells from colorectal carcinoma patients. Clin Cancer Res 6:3499–3504

    PubMed  CAS  Google Scholar 

  165. Helzer KT, Barnes HE, Day L, Harvey J, Billings PR, Forsyth A (2009) Circulating tumor cells are transcriptionally similar to the primary tumor in a murine prostate model. Cancer Res 69:7860–7866

    PubMed  CAS  Google Scholar 

  166. Kimura H, Kasahara K, Kawaishi M, Kunitoh H, Tamura T, Holloway B, Nishio K (2006) Detection of epidermal growth factor receptor mutations in serum as a predictor of the response to gefitinib in patients with non-small-cell lung cancer. Clin Cancer Res 12:3915–3921

    PubMed  CAS  Google Scholar 

  167. Maheswaran S, Sequist LV, Nagrath S, Ulkus L, Brannigan B, Collura CV, Inserra E, Diederichs S, Iafrate AJ, Bell DW, Digumarthy S, Muzikansky A, Irimia D, Settleman J, Tompkins RG, Lynch TJ, Toner M, Haber DA (2008) Detection of mutations in egfr in circulating lung-cancer cells. N Engl J Med 359:366–377

    PubMed  CAS  Google Scholar 

  168. Schmidt-Kittler O, Ragg T, Daskalakis A, Granzow M, Ahr A, Blankenstein TJ, Kaufmann M, Diebold J, Arnholdt H, Muller P, Bischoff J, Harich D, Schlimok G, Riethmuller G, Eils R, Klein CA (2003) From latent disseminated cells to overt metastasis: Genetic analysis of systemic breast cancer progression. Proc Natl Acad Sci U S A 100:7737–7742

    PubMed  CAS  Google Scholar 

  169. 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 12:5615–5621

    PubMed  CAS  Google Scholar 

  170. 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 pre-metastatic niche. Nature 438:820–827

    Google Scholar 

  171. Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132:598–611

    PubMed  CAS  Google Scholar 

  172. Balasubramanian S, Venugopal P, Sundarraj S, Zakaria Z, Majumdar AS, Ta M (2012) Comparison of chemokine and receptor gene expression between wharton’s jelly and bone marrow-derived mesenchymal stromal cells. Cytotherapy 14:26–33

    PubMed  CAS  Google Scholar 

  173. Fuchs E, Tumbar T, Guasch G (2004) Socializing with the neighbors: Stem cells and their niche. Cell 116:769–778

    PubMed  CAS  Google Scholar 

  174. Udagawa T (2008) Tumor dormancy of primary and secondary cancers. Apmis 116:615–628

    PubMed  CAS  Google Scholar 

  175. Nguyen DX (2011) Tracing the origins of metastasis. J Pathol 223:195–204

    PubMed  CAS  Google Scholar 

  176. Ansieau S, Hinkal G, Thomas C, Bastid J, Puisieux A (2008) Early origin of cancer metastases: Dissemination and evolution of premalignant cells. Cell Cycle 7:3659–3663

    PubMed  CAS  Google Scholar 

  177. Podsypanina K, Du YC, Jechlinger M, Beverly LJ, Hambardzumyan D, Varmus H (2008) Seeding and propagation of untransformed mouse mammary cells in the lung. Science 321:1841–1844

    PubMed  CAS  Google Scholar 

  178. Klein CA, Holzel D (2006) Systemic cancer progression and tumor dormancy: Mathematical models meet single cell genomics. Cell Cycle 5:1788–1798

    PubMed  CAS  Google Scholar 

  179. Backdahl M, Cohn K, Auer G, Forsslund G, Granberg PO, Lundell G, Lowhagen T, Willems JS, Zetterberg A (1985) Comparison of nuclear dna content in primary and metastatic papillary thyroid carcinoma. Cancer Res 45:2890–2894

    PubMed  CAS  Google Scholar 

  180. Psaila B, Lyden D (2009) The metastatic niche: Adapting the foreign soil. Nat Rev Cancer 9:285–293

    PubMed  CAS  Google Scholar 

  181. Zhang Y, Yang P, Wang XF (2013) Microenvironmental regulation of cancer metastasis by mirnas. Trends Cell Biol 9:239–252

    Google Scholar 

  182. Naumov GN, Akslen LA, Folkman J (2006) Role of angiogenesis in human tumor dormancy: Animal models of the angiogenic switch. Cell Cycle 5:1779–1787

    PubMed  CAS  Google Scholar 

  183. Naumov GN, Bender E, Zurakowski D, Kang SY, Sampson D, Flynn E, Watnick RS, Straume O, Akslen LA, Folkman J, Almog N (2006) A model of human tumor dormancy: An angiogenic switch from the nonangiogenic phenotype. J Natl Cancer Inst 98:316–325

    PubMed  Google Scholar 

  184. Muller-Hermelink N, Braumuller H, Pichler B, Wieder T, Mailhammer R, Schaak K, Ghoreschi K, Yazdi A, Haubner R, Sander CA, Mocikat R, Schwaiger M, Forster I, Huss R, Weber WA, Kneilling M, Rocken M (2008) TNFR1 signaling and IFN-gamma signaling determine whether t cells induce tumor dormancy or promote multistage carcinogenesis. Cancer Cell 13:507–518

    Google Scholar 

  185. Muller M, Gounari F, Prifti S, Hacker HJ, Schirrmacher V, Khazaie K (1998) Tumor dormancy in bone marrow and lymph nodes: Active control of proliferating tumor cells by cd8+ immune t cells. Cancer Res 58:5439–5446

    Google Scholar 

  186. Teng MW, Swann JB, Koebel CM, Schreiber RD, Smyth MJ (2008) Immune-mediated dormancy: An equilibrium with cancer. J Leukoc Biol 84:988–993

    PubMed  CAS  Google Scholar 

  187. Ondicova K, Mravec B (2010) Role of nervous system in cancer aetiopathogenesis. Lancet Oncol 11:596–601

    PubMed  Google Scholar 

  188. Voss MJ, Entschladen F (2010) Tumor interactions with soluble factors and the nervous system. Cell Commun Signal 8:21

    PubMed  Google Scholar 

  189. Sloan EK, Priceman SJ, Cox BF, Yu S, Pimentel MA, Tangkanangnukul V, Arevalo JM, Morizono K, Karanikolas BD, Wu L, Sood AK, Cole SW (2010) The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res 70:7042–7052

    PubMed  CAS  Google Scholar 

  190. Zanker KS (2007) The neuro-neoplastic synapse: Does it exist? Prog Exp Tumor Res 39:154–161

    PubMed  Google Scholar 

  191. Eyles J, Puaux AL, Wang X, Toh B, Prakash C, Hong M, Tan TG, Zheng L, Ong LC, Jin Y, Kato M, Prevost-Blondel A, Chow P, Yang H, Abastado JP (2010) Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest 120:2030–2039

    PubMed  CAS  Google Scholar 

  192. Fidler IJ (2003) The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer 3:453–458

    PubMed  CAS  Google Scholar 

  193. Lorusso G, Ruegg C (2008) The tumor microenvironment and its contribution to tumor evolution toward metastasis. Histochem Cell Biol 130:1091–1103

    PubMed  CAS  Google Scholar 

  194. Balkwill F, Mantovani A (2001) Inflammation and cancer: Back to Virchow? Lancet 357:539–545

    PubMed  CAS  Google Scholar 

  195. Marx J (2004) Cancer research. Inflammation and cancer: The link grows stronger. Science 306:966–968

    PubMed  CAS  Google Scholar 

  196. Walser T, Cui X, Yanagawa J, Lee JM, Heinrich E, Lee G, Sharma S, Dubinett SM (2008) Smoking and lung cancer: The role of inflammation. Proc Am Thorac Soc 5:811–815

    PubMed  Google Scholar 

  197. Scanlon EF, Suh O, Murthy SM, Mettlin C, Reid SE, Cummings KM (1995) Influence of smoking on the development of lung metastases from breast cancer. Cancer 75:2693–2699

    PubMed  CAS  Google Scholar 

  198. Murin S, Inciardi J (2001) Cigarette smoking and the risk of pulmonary metastasis from breast cancer. Chest 119:1635–1640

    PubMed  CAS  Google Scholar 

  199. Murin S, Pinkerton KE, Hubbard NE, Erickson K (2004) The effect of cigarette smoke exposure on pulmonary metastatic disease in a murine model of metastatic breast cancer. Chest 125:1467–1471

    PubMed  Google Scholar 

  200. Abrams JA, Lee PC, Port JL, Altorki NK, Neugut AI (2008) Cigarette smoking and risk of lung metastasis from esophageal cancer. Cancer Epidemiol Biomarkers Prev 17:2707–2713

    PubMed  Google Scholar 

  201. Taranova AG, Maldonado DR, Vachon CM, Jacobsen EA, Abdala-Valencia H, McGarry MP, Ochkur SI, Protheroe CA, Doyle A, Grant CS, Cook-Mills J, Birnbaumer L, Lee NA, Lee JJ (2008) Allergic pulmonary inflammation promotes the recruitment of circulating tumor cells to the lung. Cancer Res 68:8582–8589

    PubMed  CAS  Google Scholar 

  202. Kobayashi T, Todoroki T, Sato H (1987) Enhancement of pulmonary metastasis of murine fibrosarcoma NR-FS by ozone exposure. J Toxicol Environ Health 20:135–145

    Google Scholar 

  203. Adamson IY, Orr FW, Young L (1986) Effects of injury and repair of the pulmonary endothelium on lung metastasis after bleomycin. J Pathol 150:279–287

    PubMed  CAS  Google Scholar 

  204. Wu Y, Brodt P, Sun H, Mejia W, Novosyadlyy R, Nunez N, Chen X, Mendoza A, Hong SH, Khanna C, Yakar S (2010) Insulin-like growth factor-i regulates the liver microenvironment in obese mice and promotes liver metastasis. Cancer Res 70:57–67

    PubMed  CAS  Google Scholar 

  205. Harun N, Nikfarjam M, Muralidharan V, Christophi C (2007) Liver regeneration stimulates tumor metastases. J Surg Res 138:284–290

    PubMed  Google Scholar 

  206. Nicoud IB, Jones CM, Pierce JM, Earl TM, Matrisian LM, Chari RS, Gorden DL (2007) Warm hepatic ischemia-reperfusion promotes growth of colorectal carcinoma micrometastases in mouse liver via matrix metalloproteinase-9 induction. Cancer Res 67:2720–2728

    PubMed  CAS  Google Scholar 

  207. Qi K, Qiu H, Sun D, Minuk GY, Lizardo M, Rutherford J, Orr FW (2004) Impact of cirrhosis on the development of experimental hepatic metastases by b16f1 melanoma cells in c57bl/6 mice. Hepatology 40:1144–1150

    PubMed  Google Scholar 

  208. Zeamari S, Roos E, Stewart FA (2004) Tumour seeding in peritoneal wound sites in relation to growth-factor expression in early granulation tissue. Eur J Cancer 40:1431–1440

    PubMed  CAS  Google Scholar 

  209. Aoki Y, Shimura H, Li H, Mizumoto K, Date K, Tanaka M (1999) A model of port-site metastases of gallbladder cancer: The influence of peritoneal injury and its repair on abdominal wall metastases. Surgery 125:553–559

    PubMed  CAS  Google Scholar 

  210. Nagai S, Fujii T, Kodera Y, Kanda M, Sahin TT, Kanzaki A, Hayashi M, Sugimoto H, Nomoto S, Takeda S, Morita S, Nakao A (2011) Recurrence pattern and prognosis of pancreatic cancer after pancreatic fistula. Ann Surg Oncol 18:2329–2337

    PubMed  Google Scholar 

  211. Chang HY, Nuyten DS, Sneddon JB, Hastie T, Tibshirani R, Sorlie T, Dai H, He YD, Van’T VL, Bartelink H, van de Rijn M, Brown PO, van de Vijver MJ (2005) Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc Natl Acad Sci U S A 102:3738–3743

    PubMed  CAS  Google Scholar 

  212. Condeelis J, Pollard JW (2006) Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell 124:263–266

    PubMed  CAS  Google Scholar 

  213. Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, Montgomery K, Chi JT, van de Rijn M, Botstein D, Brown PO (2004) Gene expression signature of fibroblast serum response predicts human cancer progression: Similarities between tumors and wounds. PLoS Biol 2:E7

    PubMed  Google Scholar 

  214. Dauer DJ, Ferraro B, Song L, Yu B, Mora L, Buettner R, Enkemann S, Jove R, Haura EB (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24:3397–3408

    PubMed  CAS  Google Scholar 

  215. Ishizuka M, Nagata H, Takagi K, Kubota K (2010) Systemic inflammatory response associated with distant metastasis of t1 or t2 colorectal cancer. Dig Dis Sci 55:3181–3187

    PubMed  CAS  Google Scholar 

  216. Cole SW (2009) Chronic inflammation and breast cancer recurrence. J Clin Oncol 27:3418–3419

    PubMed  Google Scholar 

  217. Allin KH, Nordestgaard BG, Flyger H, Bojesen SE (2011) Elevated pre-treatment levels of plasma c-reactive protein are associated with poor prognosis after breast cancer: A cohort study. Breast Cancer Res 13:R55

    PubMed  CAS  Google Scholar 

  218. Ramaswamy S, Ross KN, Lander ES, Golub TR (2003) A molecular signature of metastasis in primary solid tumors. Nat Genet 33:49–54

    PubMed  CAS  Google Scholar 

  219. Minn AJ, Kang Y, Serganova I, Gupta GP, Giri DD, Doubrovin M, Ponomarev V, Gerald WL, Blasberg R, Massague J (2005) Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J Clin Invest 115:44–55

    PubMed  CAS  Google Scholar 

  220. Poon E, Ong SJ, Chuang XE, Lim WT, Mohd ZN, Chong TW, Al JI, Mancer K (2011) Tan MH: ‘prechronous’ Metastasis in clear cell renal cell carcinoma: A case report. J Med Case Rep 5:181

    PubMed  Google Scholar 

  221. Schneuber SE, Scholz HS, Regitnig P, Petru E, Winter R (2008) Breast metastasis 56 months before the diagnosis of primary ovarian cancer: A case study. Anticancer Res 28:3047–3050

    PubMed  Google Scholar 

  222. Furak J, Trojan I, Tiszlavicz L, Micsik T, Puskas LG (2003) Development of brain metastasis 5 years before the appearance of the primary lung cancer: “Messenger metachronous metastasis”. Ann Thorac Surg 75:1016–1017

    PubMed  Google Scholar 

  223. Briasoulis E, Pavlidis N (1997) Cancer of unknown primary origin. Oncologist 2:142–152

    PubMed  Google Scholar 

  224. OGILVY IH (1951) Pancreatic tissue in the wall of the small intestine. Aust N Z J Surg 20:224–231

    PubMed  CAS  Google Scholar 

  225. Klein CA (2008) Cancer. The metastasis cascade. Science 321:1785–1787

    PubMed  CAS  Google Scholar 

  226. de la Monte SM, Moore GW, Hutchins GM (1983) Patterned distribution of metastases from malignant melanoma in humans. Cancer Res 43:3427–3433

    PubMed  Google Scholar 

  227. Eccles SA, Welch DR (2007) Metastasis: Recent discoveries and novel treatment strategies. Lancet 369:1742–1757

    PubMed  CAS  Google Scholar 

  228. Takahashi K, Kohno T, Matsumoto S, et al (2007) Clonal and parallel evolution of primary lung cancers and their metastases revealed by molecular dissection of cancer cells. Clin Cancer Res 13:111–120

    Google Scholar 

  229. Fleming JM, Miller TC, Quinones M, Xiao Z, Xu X, Meyer MJ, Ginsburg E, Veenstra TD, Vonderhaar BK (2010) The normal breast microenvironment of premenopausal women differentially influences the behavior of breast cancer cells in vitro and in vivo. BMC Med 8:27

    PubMed  Google Scholar 

  230. Kozlowski JM (1994) Management of distant solitary recurrence in the patient with renal cancer. Contralateral kidney and other sites. Urol Clin North Am 21:601–624

    PubMed  CAS  Google Scholar 

  231. Saitoh H (1981) Distant metastasis of renal adenocarcinoma. Cancer 48:1487–1491

    PubMed  CAS  Google Scholar 

  232. Brooks JD, Teraoka SN, Malone KE, Haile RW, Bernstein L, Lynch CF, Mellemkjaer L, Duggan DJ, Reiner AS, Concannon P, Schiermeyer K, Lewinger JP, Bernstein JL, Figueiredo JC (2013) Variants in tamoxifen metabolizing genes: A case–control study of contralateral breast cancer risk in the wecare study. Int J Mol Epidemiol Genet 4:35–48

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are regretted for omitting primary references and the work of those we could not cite because of space limitations. We would like to thank editor’ careful work.

Conflict interest

The authors declare no any interests.

Author information

Authors and Affiliations

  1. 536 Hospital of PLA, 29# Xiadu street, Xining, 810007, Qinghai Province, People’s Republic of China

    Dongwei Gao

  2. Department of Radiation Oncology, Lanzhou General Hospital of PLA, 333# Southern Binhe Road, Lanzhou, 730050, Gansu Province, People’s Republic of China

    Dongwei Gao & Sha Li

Authors
  1. Dongwei Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sha Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dongwei Gao.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gao, D., Li, S. Biological resonance for cancer metastasis, a new hypothesis based on comparisons between primary cancers and metastases. Cancer Microenvironment 6, 213–230 (2013). https://doi.org/10.1007/s12307-013-0138-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12307-013-0138-y

Keywords

Search

Navigation