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01-12-2008 | Review Paper

The chick embryo chorioallantoic membrane as a model to study tumor metastasis

Published in: Angiogenesis | Issue 4/2008

Abstract

Tumor metastasis represents a major problem in the treatment of patients with different cancers. Specific phenotype and behavior of metastatic cells derive from specific molecular mechanisms involved in consecutive steps of the metastatic process. Several in vitro and in vivo experimental models have been utilized, but they cannot completely reproduce and characterize each step of the metastatic process. This review article is focused on the chick embryo chorioallantoic membrane as an in vivo model to study the metastatic process.

Ribatti D, Mangialardi G, Vacca A (2006) Stephen Paget and the ‘seed and soil’ theory of metastatic dissemination. Clin Exp Med 6:145–149. doi:10.1007/s10238-006-0117-4 PubMedCrossRef

Folkman J (1990) What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 82:4–6. doi:10.1093/jnci/82.1.4 PubMedCrossRef

Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N (2003) Angiogenesis assays: a critical overview. Clin Chem 49:32–40. doi:10.1373/49.1.32 PubMedCrossRef

Ribatti D, Vacca A, Roncali L, Dammacco F (2000) The chick chorioallantoic membrane as a model for in vivo research on anti-angiogenesis. Curr Pharm Biotechnol 1:73–82. doi:10.2174/1389201003379040 PubMedCrossRef

Ribatti D, Nico B, Vacca A, Roncali L, Burri PH, Djonov V (2001) Chorioallantoic membrane capilary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo. Anat Rec 264:317–324. doi:10.1002/ar.10021 PubMedCrossRef

Tufan AC, Satiroglu-Tufan NL (2005) The chick embryo chorioallantoic membrane as a model system for the study of tumor angiogenesis, invasion and development of anti-angiogenic agents. Curr Cancer Drug Targets 5:249–266. doi:10.2174/1568009054064624 PubMedCrossRef

Romanoff AL (1960) The avian embryo: structural and functional development. The Macmillan Company, New York

Fuchs A, Lindenbaum ES (1988) The two- and three-dimensional structure of the microcirculation of the chick chorioallantoic membrane. Acta Anat (Basel) 131:271–275. doi:10.1159/000146528 CrossRef

Ausprunk DH, Knighton DR, Folkman J (1974) Differentiation of the vascular endothelium in the chick chorioallantois: a structural and autoradiographic study. Dev Biol 38:237–247. doi:10.1016/0012-1606(74)90004-9 PubMedCrossRef

10.

Oh SJ, Jeltsch MM, Birkenhager R, McCarthy JEG, Weich HA, Christ B et al (1987) VEGF and VEGF-C: specific induction of angiogenesis and lymph angiogenesis in the differentiated avian chorioallantoic membrane. Dev Biol 188:96–109. doi:10.1006/dbio.1997.8639 CrossRef

11.

Wilting J, Neeff H, Christ B (1999) Embryonic lymph angiogenesis. Cell Tissue Res 297:1–11. doi:10.1007/s004410051328 PubMedCrossRef

12.

Wilting J, Birkenhager R, Eichmann A, Kurz H, Martony-Baron G, Marmé D et al (1996) VEGF121 induces proliferation of vascular endothelial cells and expression of flk-1 without affecting lymphatic vessels of the chorioallantoic membrane. Dev Biol 176:76–85. doi:10.1006/dbio.1996.9993 PubMedCrossRef

13.

Papoutsi M, Tomarev SI, Eichmann A, Prols F, Christ B, Wilting J (2001) Endogenous origin of the lymphatics in the avian chorioallantoic membrane. Dev Dyn 222:238–251. doi:10.1002/dvdy.1187 PubMedCrossRef

14.

Langer R, Folkman J (1976) Polymers for sustained release of proteins and other macromolecules. Nature 263:797–800. doi:10.1038/263797a0 PubMedCrossRef

15.

Wilting J, Christ B, Bokeloh M (1991) A modified chorioallantoic membrane (CAM) assay for qualitative and quantitative study of growth factors. Studies on the effects of carriers, PBS, angiogenin and bFGF. Anat Embryol (Berl) 183:259–271. doi:10.1007/BF00192214

16.

Ribatti D, Roncali L, Nico B, Bertossi M (1987) Effects of exogenous heparin on the vasculogenesis of the chorioallantoic membrane. Acta Anat (Basel) 130:257–263. doi:10.1159/000146454 CrossRef

17.

Nguyen D, Shing Y, Folkman J (1994) Quantitation of angiogenesis and anti-angiogenesis in the chick embryo chorioallantoic membrane. Microvasc Res 47:31–40. doi:10.1006/mvre.1994.1003 PubMedCrossRef

18.

Ribatti D, Nico B, Vacca A, Presta M (2006) The gelatin sponge-chorioallantoic membrane assay. Nat Prot 1:85–91. doi:10.1038/nprot.2006.13 CrossRef

19.

Hamburger V, Hamilton HL (1951) A series of normal stages in development of the chick embryo. J Morphol 88:49–92. doi:10.1002/jmor.1050880104 CrossRef

20.

Auerbach R, Kubai L, Knighton D, Folkman J (1974) A simple procedure for the long-term cultivation of chicken embryos. Dev Biol 41:391–394. doi:10.1016/0012-1606(74)90316-9 PubMedCrossRef

21.

Dugan JD Jr, Lawton MT, Glaser B, Brem H (1981) A new technique for explantation and in vitro cultivation of chicken embryos. Anat Rec 229:125–128. doi:10.1002/ar.1092290114 CrossRef

22.

Crum R, Szabo W, Folkman J (1985) A new class of steroids inhibits angiogenesis in the presence of heparin. Science 230:1375–1378. doi:10.1126/science.2416056 PubMedCrossRef

23.

Rous P, Murphy JB (1911) Tumor implantations in the developing embryo. J Am Med Assoc 56:741

24.

Murphy JB (1912) Transplantability of malignant tumors to embryos of a foreign species. J Am Med Assoc 59:874

25.

Clark ER (1920) Technique of operating on chick embryos. Science 51:371–373. doi:10.1126/science.51.1319.371 PubMedCrossRef

26.

Willier BH (1924) The endocrine glands and the development of the chick. I. The effects of thyroid grafts. Am J Anat 33:67–103. doi:10.1002/aja.1000330105 CrossRef

27.

Burnett FM (1933) A virus disease of the canary of the fowl-pox group. J Path Bact 37:107–122. doi:10.1002/path.1700370111 CrossRef

28.

Taylor A, Carmichael N, Norris T (1948) A further report on yolk sac cultivation of tumor tissue. Cancer Res 8:264PubMed

29.

Karnofsky DA, Ridgway LP, Patterson PA (1952) Tumor transplantation to the chick embryo. Ann N Y Acad Sci 35:313–329. doi:10.1111/j.1749-6632.1952.tb26547.x CrossRef

30.

Korngold L, Lipari R (1955) Tissue antigens of human tumors grown in rats, hamsters and eggs. Cancer Res 15:159–161PubMed

31.

Harris JJ (1958) The human tumors grown in the egg. Ann N Y Acad Sci 76:764–774. doi:10.1111/j.1749-6632.1958.tb54894.x PubMedCrossRef

32.

Kaufman N, Kinney TD, Mason EJ, Prieto LC (1955) Maintenance of human neoplasm on the chick chorioallantoic membrane. Am J Pathol 32:271–285

33.

Dagg CP, Karnofsky DA, Roddy J (1956) Growth of transplantable human tumors in the chick embryo and hatched chick. Cancer Res 16:589–596PubMed

34.

Locker J, Goldblatt BJ, Leighton J (1969) Hematogenous metastasis of Yoshida Ascites Hepatoma in the chick embryo liver: ultrastructural changes in tumor cells. Cancer Res 29:1244–1253

35.

Ossowski L, Reich E (1980) Experimental model for quantitative study of metastasis. Cancer Res 40:2300–2309PubMed

36.

Yu W, Kim J, Ossowski L (1997) Reduction in surface urokinase receptor forces malignant cells into a protracted state of dormancy. J Cell Biol 137:767–777. doi:10.1083/jcb.137.3.767 PubMedCrossRef

37.

Kim J, Yu W, Kovalski K, Ossowski L (1998) Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell 94:353–362. doi:10.1016/S0092-8674(00)81478-6 PubMedCrossRef

38.

Chambers AF, Sharif R, Ling V (1982) A model system for studying metastasis using the embryonic chick. Cancer Res 42:4018–4025PubMed

39.

MacDonald IC, Schmidt EE, Morris VL, Chambers AF, Groom AC (1992) Intravital videomicroscopy of the chorioallantoic microcirculation: a model system for studying metastasis. Microvasc Res 44:185–199. doi:10.1016/0026-2862(92)90079-5 PubMedCrossRef

40.

Koop S, Schmidt EE, MacDonald IC, Morris VL, Khokha R, Grattan M et al (1996) Independence of metastatic ability and extravasation: metastatic ras-transformed and control fibroblasts extravasate equally well. Proc Natl Acad Sci USA 93:11080–11084. doi:10.1073/pnas.93.20.11080 PubMedCrossRef

41.

Khoka R, Zimmer MJ, Wilson SM, Chambers AF (1992) Upregulation of TIMP-1 expression in B16–F10 melanoma cells suppresses their metastatic ability in chick embryo. Clin Exp Metastasis 10:365–370. doi:10.1007/BF00133464 CrossRef

42.

Brooks PC, Lin J-M, French DL, Quigley JP (1993) Subtractive immunization yields monoclonal antibodies that specifically inhibit metastasis. J Cell Biol 122:1351–1359. doi:10.1083/jcb.122.6.1351 PubMedCrossRef

43.

Zijlstra A, Mellor R, Panzarella G, Aimes RT, Marchenko ND, Quigley J (2002) A quantitative analysis of rate-limiting steps in the metastatic cascade using human-specific real-time polymerase chain reaction. Cancer Res 62:7083–7092PubMed

44.

Mira E, Lacalle RA, Gomez-Mouton C, Leonardo E, Manes S (2002) Quantitative determination of tumor cell intravasation in a real-time polymerase chain reaction-based assay. Clin Exp Metastasis 19:313–318. doi:10.1023/A:1015563031769 PubMedCrossRef

45.

Van der Horst EH, Leupold JH, Schubbert R, Ulrich A, Allgayer H (2004) Taqman-based quantitation of invasive cells in the chick embryo metastasis assay. Biotechnique 37:940–945

46.

Ossowski L (1988) Plasminogen activator dependent pathways in the dissemination of human tumor cells in the chick embryo. Cell 52:321–328. doi:10.1016/S0092-8674(88)80025-4 PubMedCrossRef

47.

Ossowski L (1988) In vivo invasion of modified chorioallantoic membrane by tumor cells: the role of cell surface-bound urokinase. J Cell Biol 107:2437–2445. doi:10.1083/jcb.107.6.2437 PubMedCrossRef

48.

Sabeh F, Ota I, Holmbeck K, Birkedal-Hansen H, Soloway P, Balbin M et al (2004) Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 167:769–781. doi:10.1083/jcb.200408028 PubMedCrossRef

49.

Deryugina EI, Zijlstra A, Partridge JJ, Kupriyanova TA, Madsen MA, Papagiannakopoulos T et al (2005) Unexpected effect of matrix metalloproteinase down-regulation on vascular intravasation and metastasis of human fibrosarcoma cells selected in vivo for high rates of dissemination. Cancer Res 65:10959–10969. doi:10.1158/0008-5472.CAN-05-2228 PubMedCrossRef

50.

Shioda T, Munn LL, Fenner MH, Jain RK, Isselbacher KJ (1997) Early events of metastasis in the microcirculation involve changes in gene expression of cancer cells tracking mRNA levels of metastasizing cancer cells in the chick embryo chorioallantoic membrane. Am J Pathol 150:2099–2112PubMed

51.

Kobayashi T, Koshida K, Endo Y, Imao T, Uchibayashi T, Sasaki T et al (1998) A chick embryo model for metastatic human prostate cancer. Eur Urol 34:154–160. doi:10.1159/000019702 PubMedCrossRef

52.

Bobek V, Plachy J, Pinterova D, Kolostova K, Boubelik M, Jiang P et al (2004) Development of a green fluorescent protein metastatic-cancer chick-embryo drug-screen model. Clin Exp Metastasis 21:347–352. doi:10.1023/B:CLIN.0000046138.58210.31 PubMedCrossRef

53.

Fidler IJ (1975) Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 35:218–224PubMed

54.

Chambers AF, Schmidt EE, MacDonald IC, Morris VL, Groom AC (1992) Early steps in hematogenous metastasis of B16F1 melanoma cells in chick embryo studied by high-resolution intravital videomicroscopy. J Natl Cancer Inst 84:797–803. doi:10.1093/jnci/84.10.797 PubMedCrossRef

55.

Koop S, Khokha R, Schmidt EE, MacDonald IC, Morris VL, Chambers AF et al (1994) Overexpression of metalloproteinase inhibitor in B16F10 cells does not affect extravasation but reduces tumor growth. Cancer Res 54:4791–4797PubMed

56.

Koop S, MacDonald IC, Luzzi K, Schmidt EE, Morris VL, Grattan M et al (1995) Fate of melanoma cells entering the microcirculation: over 80% survive and extravasate. Cancer Res 55:2520–2523PubMed

57.

Taizi M, Deutsch VR, Letiner A, Ohana A, Goldtsein RS (2006) A novel and rapid in vivo system for testing therapeutics on human leukemias. Exp Hematol 34:1698–1708. doi:10.1016/j.exphem.2006.07.005 PubMedCrossRef

58.

Gordon J, Quigley J (1986) Early spontaneous metastasis in the human epidermoid carcinoma Hep3/chick embryo model: contribution of incidental colonization. Int J Cancer 38:437–444. doi:10.1002/ijc.2910380321 PubMedCrossRef

59.

Lugassy C, Barnhill RL (2007) Angiotropic melanoma and extravascular migratory metastasis: a review. Adv Anat Pathol 14:195–201. doi:10.1097/PAP.0b013e31805048d9 PubMedCrossRef

60.

Hagedorn M, Javerzat S, Gilges D, Meyre A, de Lafarge B, Eichmann A et al (2005) Accessing key steps of human tumor progression in vivo by using an avian embryo model. Proc Natl Acad Sci USA 102:1643–1648. doi:10.1073/pnas.0408622102 PubMedCrossRef

61.

Papoutsi M, Sleeman JP, Wilting GJ (2001) Interaction of rat tumor cells with blood vessels and lymphatics of the avian chorioallantoic membrane. Microsc Res Tech 55:100–107. doi:10.1002/jemt.1161 PubMedCrossRef

62.

Papoutsi M, Siemeister G, Weindel K, Tomarev SI, Kurz H, Schachtele C et al (2000) Active interaction of human A375 melanoma cells with the lymphatics in vivo. Histochem Cell Biol 114:373–385PubMed

63.

Ribatti D, Vacca A, Roncali L, Dammacco F (1996) The chick embryo chorioallantoic membrane as a model for in vivo research on angiogenesis. Int J Dev Biol 40:1189–1197PubMed

64.

Ribatti D, Nico B, Pezzolo A, Vacca A, Meazza R, Cinti R et al (2006) Angiogenesis in a human neuroblastoma xenograft model: mechanisms and inhibition by tumour-derived interferon-gamma. Br J Cancer 94:1845–1852PubMedCrossRef

65.

Ribatti D, Alessandri G, Vacca A, Iurlaro M, Ponzoni M (1998) Human neuroblastoma cells produce extracellular matrix-degrading enzymes, induce endothelial cell proliferation and are angiogenic in vivo. Int J Cancer 77:449–454PubMedCrossRef

Title: The chick embryo chorioallantoic membrane as a model to study tumor metastasis
Publication date: 01-12-2008
Published in: Angiogenesis / Issue 4/2008
Print ISSN: 0969-6970
Electronic ISSN: 1573-7209
DOI: https://doi.org/10.1007/s10456-008-9117-1

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