Regulation of VEGF and VEGF receptor expression in the rodent mammary gland during pregnancy, lactation, and involution

Developmental Dynamics

Volumn 218, Issue 3, 2000, Pages 507-524

  Pepper, Michael S ^a   Baetens, Danielle ^a   Mandriota, Stefano J ^a   Di Sanza, Corinne ^a   Oikemus, Sarah ^b   Lane, Timothy F ^c   Soriano, Jesus V ^a,d   Montesano, Roberto ^a   Iruela Arispe, M Luisa ^b  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Angiogenesis; Breast; Growth factor; Vascular permeability

Indexed keywords

GROWTH FACTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; INVOLUTION; LACTATION; MAMMARY GLAND; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS;

ADULT; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BLOTTING, NORTHERN; CAPILLARIES; CELL LINE; ENDOTHELIAL GROWTH FACTORS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LACTATION; LYMPHOKINES; MAMMARY GLANDS, ANIMAL; MICE; MILK, HUMAN; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PHYSIOLOGIC; PREGNANCY; RATS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RNA; SEQUENCE ALIGNMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTORS; WEANING;

ANIMALIA; RODENTIA;

EID: 0033940428     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/1097-0177(200007)218:3<507::AID-DVDY1012>3.0.CO;2-5     Document Type: Article

References (53)

1. Alroy J, Goyal V, Skutelsky E. 1987. Lectin histochemistry of mammalin endothelium. Histochem 86:603-607.
2. Baribault H, Price J, Miyai K, Oshima RG. 1993. Mid-gestational lethality in mice lacking keratin 8. Genes Dev 7:1191-1202.
3. Breier G, Albrecht U, Strerrer S, Risau W. 1992. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114:521-532.
4. Brown LF, Berse B, Jackman RW, Tognazzi K, Guidi AJ, Dvorak HF, Senger DR, Connolly JL, Schnitt SJ. 1995. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in breast cancer. Hum Pathol 26:86-91.
5. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
6. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
7. Claffey KP, Wilkison WO, Spigelman BM. 1992. Vascular endothelial growth factor. Regulation by cell differentation and activated second messenger pathways. J Biol Chem 267:16317-16322.
8. Conn G, Bayne ML, Soderman DD, Kwok PW, Sullivan KA, Palisi TM, Hope DA, Thomas KA. 1990. Amino acid and cDNA sequences of a vascular endothelial cell mitogen that is homologous to platelet-derived growth factor. Proc Natl Acad Sci USA 87:2628-2632.
9. Daniel CW, Silberstein GB. 1987. Postnatal development of the rodent mammary gland. In: Neville MC and Daniel CW, editors. The mammary gland. New York: Plenum Press. p 3-36.
10. Duijvestijn AM, van Goor H, Klatter F, Majoor GD, van Bussel E, van Breda Vriesman PJC. 1992. Antibodies defining rat endothelial cells: RECA-1, a pan-endothelial cell-specific monoclonal antibody. Lab Invest 66:459-466.
11. Dvorak HF, Brown LF, Detmar M, Dvorak AM. 1995. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 146: 1029-1039.
12. Feng D, Nagy JA, Pyne K, Hammel I, Dvorak HF, Dvorak AM. 1999. Pathways of macromolecular extravasation across microvascular endothelium in response to VPF/VEGF and other vasoactive mediators. Microcirculation 6:23-44.
13. Ferrara N. 1999. Role of vascular endothelial growth factor in the regulation of angiogenesis. Kidney Int 56:794-814.
14. Findlay JK. 1986. Angiogenesis in reproductive tissues. J Endocrinol 111:357-366.
15. Finnerty H, Kelleher K, Morris GE, Bean K, Merberg DM, Kriz, R, Morris JC, Sookdeo H, Turner KJ, Wood CR. 1993. Molecular cloning of murine FLT and FLT4. Oncogene 8:2293-2298.
16. Gasparini G, Toi M, Gion M, Verderio P, Dittadi R, Hanatani M, Matsubara I, Vinante O, Bonoldi E, Boracchi P, Gatti C, Suzuki H, Tominaga T. 1997. Prognostic significance of vascular endothelial growth factor protein in node-negative breast carcinoma. J Nat Cancer Inst 89:139-147.
17. Gavin BJ, McMahon AP. 1992. Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol Cell Biol 12:2418-2423.
18. Greb RR, Maier I, Wallwiener D, Kiesel L. 1999. Vascular endothelial growth factor A (VEGF-A) mRNA expression levels decrease after menopause in normal breast tissue but not in breast cancer lesions. Br J Cancer 81:225-231.
19. Hlatky L, Tsionou C, Hahnfeldt P, Coleman CN. 1994. Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res 54:6083-6086.
20. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K. 1996. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15:290-298.
21. Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsch M, Joukov V, Alitalo K. 1996. VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 122:3829-3837.
22. Lee J, Gray A, Yuan J, Luoh SM, Avraham H, Wood WI. 1996. Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA 93:1988-1992.
23. Lichtenbeld HC, Barendsz-Janson AF, van Essen H, Struijker Boudier H, Griffioen AW, Hillen HF. 1998. Angiogenic potential of malignant and non-malignant human breast tissues in an in vivo angiogenesis model. Int J Cancer 77:455-459.
24. Matsumoto K, Nakamura T. 1996. Emerging multipotent aspects of hepatocyte growth factor. J Biochem 119:591-600.
25. Matsumoto M, Nishinakagawa H, Kurohmaru M, Hayashi Y, Otsuka J. 1992. Pregnancy and lactation affect the microvasculature of the mammary gland in mice. J Vet Med Sci 54:937-943.
26. Matsumoto M, Kurohmaru M, Hayashi Y, Nishinakagawa H, Otsuka J. 1994. Permeability of mammary gland capillaries to ferritin in mice. J Vet Med Sci 56:65-70.
27. Matthews W, Jordan CT, Gavin, M, Jenkins NA, Copeland NG, Le-mischka IR 1991. A receptor tyrosine kinase cDNA isolated from a population of enriched primitive hematopoietic cells and exhibiting close genetic linkage to c-kit. Proc Natl Acad Sci USA 88:9026-9030.
28. Nakahasi HL, Qasba PK. 1979. Quantitation of milk proteins and their mRNAs in rat mammary gland at various stages of gestation and lactation. J Biol Chem 254:6016-6025.
29. Nakamura J, Lu Q, Aberdeen G, Albrecht E, Brodie A. 1999. The effect of estrogen on aromatase and vascular endothelial growth factor messenger ribonucleic acid in the normal nonhuman primate mammary gland. J Clin Endocrinol Metab 84:1432-1437.
30. Newman PJ, Berndt MC, Gorski J, White GC 2d, Lyman S, Paddock C, Muller WA. 1990. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247:1219-1222.
31. Obermair A, Kucera E, Mayerhofer K, Speiser P, Seifert M, Czerwenka K, Kaider A, Leodolter S, Kainz C, Zeillinger R. 1997. Vascular endothelial growth factor (VEGF) in human breast cancer: correlation with disease-free survival. Int J Cancer 74:455-458.
32. Owens RB, Smith HS, Hackett AJ. 1974. Epithelial cell cultures from normal glandular tissue of mice. J Natl Cancer Inst 53:261-269.
33. Pajusola K, Aprelikova O, Armstrong E, Morris S, Alitalo K. 1993. Two human FLT4 receptor tyrosine kinase isoforms with distinct carboxy terminal tails are produced by alternative processing of primary transcripts. Oncogene 8:2931-2937.
34. Pepper MS, Belin D, Montesano R, Orci L, Vassalli JD. 1990. Transforming growth factor-beta 1 modulates basic fibroblast growth factor-induced proteolytic and angiogenic properties of endothelial cells in vitro. J Cell Biol 111:743-755.
35. Pepper MS, Soriano JV, Menoud PA, Sappino AP, Orci L, Montesano R. 1995. Modulation of hepatocyte growth factor and c-met in the rat mammary gland during pregnancy, lactation, and involution. Exp Cell Res 219:204-210.
36. Sappino AP, Huarte J, Belin D, Vassalli JD. 1989. Plasminogen activators in tissue remodeling and invasion: mRNA localization in mouse ovaries and implanting embryos. J Cell Biol 109:2471-2479.
37. Siafakas CG, Anatolitou F, Fusunyan RD, Walker WA, Sanderson IR. 1999. Vascular endothelial growth factor (VEGF) is present in human breast milk and its receptor is present on intestinal epithelial cells. Pediatr Res 45:652-657.
38. Soemarwoto IN, Bern HA. 1958. The effect of hormones on the vascular pattern of the mouse mammary gland. Am J Anat 103:403-435.
39. Soriano JV, Pepper MS, Nakamura T, Orci L, Montesano R. 1995. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J Cell Sci 108:413-430.
40. Stacker SA, Achen MG. 1999. The vascular endothelial growth factor family: signalling for vascular development. Growth Factors 17:1-11.
41. Stewart RJ, Kashxur TS, Marsden PA. 1996. Vascular endothelial platelet endothelial adhesion molecule-1 (PECAM-1) expression is decreased by TNF-alpha and IFN-gamma. Evidence for cytokine-induced destabilization of messenger ribonucleic acid transcripts in bovine endothelial cells. J Immunol 156:1221-1228.
42. Stirling JW, Chandler JA. 1976. The fine structure of the normal, resting terminal ductal-lobular unit of the female breast. Virchows Arch A Pathol Anat Histol 372:205-226.
43. Thomasset N, Lochter A, Sympson CJ, Lund LR, Williams DR, Behrendtsen O, Werb Z, Bissell, MJ 1998. Expression of autoactivated stromelysin-1 in mammary glands of transgenic mice leads to a reactive stroma during early development. Am J Pathol 153:457-467.
44. Turner CW, Gomez ET. 1933. The normal development of the mammary gland in the male and female albino mouse. Res Bull Mo Agric Exper Sta 182.
45. Valtola R, Salven P, Heikkila P, Taipale J, Joensuu H, Rehn M, Pihlajaniemi T, Weich H, deWaal R, Alitalo K. 1999. VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am J Pathol 154:1381-1390.
46. Veikkola T, Alitalo K. 1999. VEGFs, receptors and angiogenesis. Sem Cancer Biol 9:211-220.
47. Wahl HM. 1915. Development of the blood vessels of the mammary gland in the rabbit. Am J Anat 18:515-524.
48. Weidner N, Semple JP, Welch WR, Folkman J. 1991. Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N Engl J Med 324:1-8.
49. Wen Y, Edelman JL, Kang T, Zeng N, Sachs G. 1998. Two functional forms of vascular endothelial growth factor receptor-2/Flk-1 mRNA are expressed in normal rat retina. J Biol Chem 273:2090-2097.
50. Xie Y, Muller WA. 1993. Molecular cloning and adhesive properties of murine platelet/endothelial cell adhesion molecule 1. Proc Natl Acad Sci USA 90:5569-5573.
51. Yamane A, Seetharam L, Yamaguchi S, Gotoh N, Takahashi T, Neufeld G, Shibuya M. 1994. A new communication system between hepatocytes and sinusoidal endothelial cells in liver through vascular endothelial growth factor and Flt tyrosine kinase receptor family (Flt-1 and KDR/Flk-1). Oncogene 9:2683-2690.
52. Yang Y, Spitzer E, Meyer D, Sachs M, Niemann C, Hartmann G, Weidner KM, Birchmeier C, Birchmeier W. 1995. Sequential requirement of hepatocyte growth factor and neuregulin in the morphogenesis and differentiation of the mammary gland. J Cell Biol 131:215-226.
53. Yasugi T, Kaido T, Uehara Y. 1989. Changes in density and architecture of microvessels of the rat mammary gland during pregnancy and lactation. Arch Histol Cytol 52:115-122.