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Journal of Mammary Gland Biology and Neoplasia

Published in:

01-03-2008

Role of Prolactin and Vasoinhibins in the Regulation of Vascular Function in Mammary Gland

Authors: Carmen Clapp, Stéphanie Thebault, Gonzalo Martínez de la Escalera

Published in: Journal of Mammary Gland Biology and Neoplasia | Issue 1/2008

Abstract

The formation of new blood vessels has become a major focus of mammary gland research stimulated by the therapeutic opportunities of controlling angiogenesis in breast cancer. Normal growth and involution of the mammary gland are profoundly affected by the expansion and regression of blood vessels, whereas dysregulation of angiogenesis is characteristic of breast cancer growth and metastasis. Prolactin stimulates the growth and differentiation of the mammary gland under normal conditions, but its role in breast cancer is controversial. Its action is complicated by the fact that prolactin itself is angiogenic, but proteases cleave prolactin to generate vasoinhibins, a family of peptides that act on endothelial cells to suppress angiogenesis and vasodilation and to promote apoptosis-mediated vascular regression. This review summarizes our current knowledge about the vascular effects of prolactin and the generation and action of vasoinhibins, and discusses their possible contribution to the regulation of blood vessels in the normal and malignant mammary gland.

Hovey RC, Trott JF, Vonderhaar BK. Establishing a framework for the functional mammary gland: from endocrinology to morphology. J Mammary Gland Biol Neoplasia 2002;7(1):17–38.PubMed

Silberstein GB. Postnatal mammary gland morphogenesis. Microsc Res Tech 2001;52(2):155–62.PubMed

Stein T, Salomonis N, Gusterson BA. Mammary gland involution as a multi-step process. J Mammary Gland Biol Neoplasia 2007;12(1):25–35.PubMed

Folkman J. Angiogenesis. Annu Rev Med 2006;57:1–18.PubMed

Liekens S, De Clercq E, Neyts J. Angiogenesis: regulators and clinical applications. Biochem Pharmacol 2001;61(3):253–70.PubMed

Horseman ND, Zhao W, Montecino-Rodriguez E, Tanaka M, Nakashima K, Engle SJ, et al. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. Embo J 1997;16(23):6926–35.PubMed

Neville MC, McFadden TB, Forsyth I. Hormonal regulation of mammary differentiation and milk secretion. J Mammary Gland Biol Neoplasia 2002;7(1):49–66.PubMed

Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 1997;11(2):167–78.PubMed

Vonderhaar BK. Prolactin involvement in breast cancer. Endocr Relat Cancer 1999;6(3):389–404.PubMed

10.

Clevenger CV, Furth PA, Hankinson SE, Schuler LA. The role of prolactin in mammary carcinoma. Endocr Rev 2003;24(1):1–27.PubMed

11.

Clapp C, Aranda J, Gonzalez C, Jeziorski MC, Martinez de la Escalera G. Vasoinhibins: endogenous regulators of angiogenesis and vascular function. Trends Endocrinol Metab 2006;17(8):301–7.PubMed

12.

Corbacho AM, Martinez De La Escalera G, Clapp C. Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol 2002;173(2):219–38.PubMed

13.

Hadsell DL. The insulin-like growth factor system in normal mammary gland function. Breast Dis 2003;17:3–14.PubMed

14.

Matsumoto M, Nishinakagawa H, Kurohmaru M, Hayashi Y, Otsuka J. Pregnancy and lactation affect the microvasculature of the mammary gland in mice. J Vet Med Sci 1992;54(5):937–43.PubMed

15.

Djonov V, Andres AC, Ziemiecki A. Vascular remodelling during the normal and malignant life cycle of the mammary gland. Microsc Res Tech 2001;52(2):182–9.PubMed

16.

Richert MM, Schwertfeger KL, Ryder JW, Anderson SM. An atlas of mouse mammary gland development. J Mammary Gland Biol Neoplasia 2000;5(2):227–41.PubMed

17.

Yasugi T, Kaido T, Uehara Y. Changes in density and architecture of microvessels of the rat mammary gland during pregnancy and lactation. Arch Histol Cytol 1989;52(2):115–22.PubMed

18.

Abdul Awal M, Matsumoto M, Toyoshima Y, Nishinakagawa H. Ultrastructural and morphometrical studies on the endothelial cells of arteries supplying the abdomino-inguinal mammary gland of rats during the reproductive cycle. J Vet Med Sci 1996;58(1):29–34.PubMed

19.

Baxter FO, Neoh K, Tevendale MC. The beginning of the end: death signaling in early involution. J Mammary Gland Biol Neoplasia 2007;12(1):3–13.PubMed

20.

Walker NI, Bennett RE, Kerr JF. Cell death by apoptosis during involution of the lactating breast in mice and rats. Am J Anat 1989;185(1):19–32.PubMed

21.

Benaud C, Dickson RB, Thompson EW. Roles of the matrix metalloproteinases in mammary gland development and cancer. Breast Cancer Res Treat 1998;50(2):97–116.PubMed

22.

Medh RD, Thompson EB. Hormonal regulation of physiological cell turnover and apoptosis. Cell Tissue Res 2000;301(1):101–24.PubMed

23.

Busso N, Huarte J, Vassalli JD, Sappino AP, Belin D. Plasminogen activators in the mouse mammary gland. Decreased expression during lactation. J Biol Chem 1989;264(13):7455–7.PubMed

24.

Miller KD, Dul CL. Breast cancer: the role of angiogenesis and antiangiogenic therapy. Hematol Oncol Clin North Am 2004;18(5):1071–86. ix.PubMed

25.

Schneider BP, Miller KD. Angiogenesis of breast cancer. J Clin Oncol 2005;23(8):1782–90.PubMed

26.

Brem SS, Gullino PM, Medina D. Angiogenesis: a marker for neoplastic transformation of mammary papillary hyperplasia. Science 1977;195(4281):880–2.PubMed

27.

Jensen HM, Chen I, DeVault MR, Lewis AE. Angiogenesis induced by “normal” human breast tissue: a probable marker for precancer. Science 1982;218(4569):293–5.PubMed

28.

Strum JM. Angiogenic responses elicited from chorioallantoic membrane vessels by neoplastic, preneoplastic, and normal mammary tissues from GR mice. Am J Pathol 1983;111(3):282–7.PubMed

29.

Lichtenbeld HC, Barendsz-Janson AF, van Essen H, Struijker Boudier H, Griffioen AW, Hillen HF. Angiogenic potential of malignant and non-malignant human breast tissues in an in vivo angiogenesis model. Int J Cancer 1998;77(3):455–9.PubMed

30.

Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 2001;93(4):266–76.PubMed

31.

Richard DE, Berra E, Pouyssegur J. Angiogenesis: how a tumor adapts to hypoxia. Biochem Biophys Res Commun 1999;266(3):718–22.PubMed

32.

Tenan M, Fulci G, Albertoni M, Diserens AC, Hamou MF, El Atifi-Borel M, et al. Thrombospondin-1 is downregulated by anoxia and suppresses tumorigenicity of human glioblastoma cells. J Exp Med 2000;191(10):1789–98.PubMed

33.

Bos R, Zhong H, Hanrahan CF, Mommers EC, Semenza GL, Pinedo HM, et al. Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J Natl Cancer Inst 2001;93(4):309–14.PubMed

34.

Zhang HT, Scott PA, Morbidelli L, Peak S, Moore J, Turley H, et al. The 121 amino acid isoform of vascular endothelial growth factor is more strongly tumorigenic than other splice variants in vivo. Br J Cancer 2000;83(1):63–8.PubMed

35.

McLeskey SW, Zhang L, Kharbanda S, Kurebayashi J, Lippman ME, Dickson RB, et al. Fibroblast growth factor overexpressing breast carcinoma cells as models of angiogenesis and metastasis. Breast Cancer Res Treat 1996;39(1):103–17.PubMed

36.

Kim KS, Park YS. Antitumor effects of angiostatin K1–3 and endostatin genes coadministered by the hydrodynamics-based transfection method. Oncol Res 2005;15(7–8):343–50.PubMed

37.

Zou Z, Anisowicz A, Hendrix MJ, Thor A, Neveu M, Sheng S, et al. Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science 1994;263(5146):526–9.PubMed

38.

Ek ET, Dass CR, Contreras KG, Choong PF. Pigment epithelium-derived factor overexpression inhibits orthotopic osteosarcoma growth, angiogenesis and metastasis. Cancer Gene Ther 2007;14(7):616–26.PubMed

39.

Uzzan B, Nicolas P, Cucherat M, Perret GY. Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res 2004;64(9):2941–55.PubMed

40.

Guinebretiere JM, Le Monique G, Gavoille A, Bahi J, Contesso G. Angiogenesis and risk of breast cancer in women with fibrocystic disease. J Natl Cancer Inst 1994;86(8):635–6.PubMed

41.

Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis–correlation in invasive breast carcinoma. N Engl J Med 1991;324(1):1–8.PubMedCrossRef

42.

Weidner N, Folkman J, Pozza F, Bevilacqua P, Allred EN, Moore DH, et al. Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst 1992;84(24):1875–87.PubMed

43.

Dabrosin C. Sex steroid regulation of angiogenesis in breast tissue. Angiogenesis 2005;8(2):127–36.PubMed

44.

Rossiter H, Barresi C, Ghannadan M, Gruber F, Mildner M, Fodinger D, et al. Inactivation of VEGF in mammary gland epithelium severely compromises mammary gland development and function. Faseb J 2007;21(14):3994–4004.PubMed

45.

Bando H. Vascular endothelial growth factor and bevacitumab in breast cancer. Breast Cancer 2007;14(2):163–73.PubMed

46.

Hyder SM, Nawaz Z, Chiappetta C, Stancel GM. Identification of functional estrogen response elements in the gene coding for the potent angiogenic factor vascular endothelial growth factor. Cancer Res 2000;60(12):3183–90.PubMed

47.

Wu J, Richer J, Horwitz KB, Hyder SM. Progestin-dependent induction of vascular endothelial growth factor in human breast cancer cells: preferential regulation by progesterone receptor B. Cancer Res 2004;64(6):2238–44.PubMed

48.

Miele C, Rochford JJ, Filippa N, Giorgetti-Peraldi S, Van Obberghen E. Insulin and insulin-like growth factor-I induce vascular endothelial growth factor mRNA expression via different signaling pathways. J Biol Chem 2000;275(28):21695–702.PubMed

49.

Goldhar AS, Vonderhaar BK, Trott JF, Hovey RC. Prolactin-induced expression of vascular endothelial growth factor via Egr-1. Mol Cell Endocrinol 2005;232(1–2):9–19.PubMed

50.

Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 1997;138(3):707–17.PubMed

51.

Yamauchi M, Imajoh-Ohmi S, Shibuya M. Novel antiangiogenic pathway of thrombospondin-1 mediated by suppression of the cell cycle. Cancer Sci 2007;98(9):1491–7.PubMed

52.

Nor JE, Mitra RS, Sutorik MM, Mooney DJ, Castle VP, Polverini PJ. Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. J Vasc Res 2000;37(3):209–18.PubMed

53.

Zhang M, Volpert O, Shi YH, Bouck N. Maspin is an angiogenesis inhibitor. Nat Med 2000;6(2):196–9.PubMed

54.

Shao ZM, Radziszewski WJ, Barsky SH. Tamoxifen enhances myoepithelial cell suppression of human breast carcinoma progression in vitro by two different effector mechanisms. Cancer Lett 2000;157(2):133–44.PubMed

55.

Mirkin S, Wong BC, Archer DF. Effects of 17beta-estradiol, progesterone, synthetic progestins, tibolone, and raloxifene on vascular endothelial growth factor and Thrombospondin-1 messenger RNA in breast cancer cells. Int J Gynecol Cancer 2006;16(2):560–3.PubMed

56.

Uray IP, Liang Y, Hyder SM. Estradiol down-regulates CD36 expression in human breast cancer cells. Cancer Lett 2004;207(1):101–7.PubMed

57.

Li Z, Shi HY, Zhang M. Targeted expression of maspin in tumor vasculatures induces endothelial cell apoptosis. Oncogene 2005;24(12):2008–19.PubMed

58.

Volpert OV, Stellmach V, Bouck N. The modulation of thrombospondin and other naturally occurring inhibitors of angiogenesis during tumor progression. Breast Cancer Res Treat 1995;36(2):119–26.PubMed

59.

Rodriguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, Iruela-Arispe ML. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc Natl Acad Sci U S A 2001;98(22):12485–90.PubMed

60.

van Hinsbergh VW, Engelse MA, Quax PH. Pericellular proteases in angiogenesis and vasculogenesis. Arterioscler Thromb Vasc Biol 2006;26(4):716–28.PubMed

61.

Yoon SO, Park SJ, Yun CH, Chung AS. Roles of matrix metalloproteinases in tumor metastasis and angiogenesis. J Biochem Mol Biol 2003;36(1):128–37.PubMed

62.

Briozzo P, Badet J, Capony F, Pieri I, Montcourrier P, Barritault D, et al. MCF7 mammary cancer cells respond to bFGF and internalize it following its release from extracellular matrix: a permissive role of cathepsin D. Exp Cell Res 1991;194(2):252–9.PubMed

63.

Liaudet-Coopman E, Beaujouin M, Derocq D, Garcia M, Glondu-Lassis M, Laurent-Matha V, et al. Cathepsin D: newly discovered functions of a long-standing aspartic protease in cancer and apoptosis. Cancer Lett 2006;237(2):167–79.PubMed

64.

Macotela Y, Aguilar MB, Guzman-Morales J, Rivera JC, Zermeno C, Lopez-Barrera F, et al. Matrix metalloproteases from chondrocytes generate an antiangiogenic 16 kDa prolactin. J Cell Sci 2006;119(Pt 9):1790–800.PubMed

65.

Pepper MS. Extracellular proteolysis and angiogenesis. Thromb Haemost 2001;86(1):346–55.PubMed

66.

Gaytan F, Morales C, Bellido C, Aguilar E, Sanchez-Criado JE. Role of prolactin in the regulation of macrophages and in the proliferative activity of vascular cells in newly formed and regressing rat corpora lutea. Biol Reprod 1997;57(2):478–86.PubMed

67.

Struman I, Bentzien F, Lee H, Mainfroid V, D’Angelo G, Goffin V, et al. Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis. Proc Natl Acad Sci U S A 1999;96(4):1246–51.PubMed

68.

Clapp C, Martial JA, Guzman RC, Rentier-Delure F, Weiner RI. The 16-kilodalton N-terminal fragment of human prolactin is a potent inhibitor of angiogenesis. Endocrinology 1993;133(3):1292–9.PubMed

69.

Ge G, Fernandez CA, Moses MA, Greenspan DS. Bone morphogenetic protein 1 processes prolactin to a 17-kDa antiangiogenic factor. Proc Natl Acad Sci U S A 2007;104(24):10010–5.PubMed

70.

Ueda E, Ozerdem U, Chen YH, Yao M, Huang KT, Sun H, et al. A molecular mimic demonstrates that phosphorylated human prolactin is a potent anti-angiogenic hormone. Endocr Relat Cancer 2006;13(1):95–111.PubMed

71.

Ko JY, Ahn YL, Cho BN. Angiogenesis and white blood cell proliferation induced in mice by injection of a prolactin-expressing plasmid into muscle. Mol Cells 2003;15(2):262–70.PubMed

72.

Hilfiker-Kleiner D, Kaminski K, Podewski E, Bonda T, Schaefer A, Sliwa K, et al. A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. Cell 2007;128(3):589–600.PubMed

73.

Clapp C, Lopez-Gomez FJ, Nava G, Corbacho A, Torner L, Macotela Y, et al. Expression of prolactin mRNA and of prolactin-like proteins in endothelial cells: evidence for autocrine effects. J Endocrinol 1998;158(1):137–44.PubMed

74.

Grosdemouge I, Bachelot A, Lucas A, Baran N, Kelly PA, Binart N. Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod Biol Endocrinol 2003;1:12.PubMed

75.

Duenas Z, Torner L, Corbacho AM, Ochoa A, Gutierrez-Ospina G, Lopez-Barrera F, et al. Inhibition of rat corneal angiogenesis by 16-kDa prolactin and by endogenous prolactin-like molecules. Invest Ophthalmol Vis Sci 1999;40(11):2498–505.PubMed

76.

Ochoa A, Montes de Oca P, Rivera JC, Duenas Z, Nava G, de La Escalera GM, et al. Expression of prolactin gene and secretion of prolactin by rat retinal capillary endothelial cells. Invest Ophthalmol Vis Sci 2001;42(7):1639–45.PubMed

77.

Clapp C, Weiner RI. A specific, high affinity, saturable binding site for the 16-kilodalton fragment of prolactin on capillary endothelial cells. Endocrinology 1992;130(3):1380–6.PubMed

78.

Merkle CJ, Schuler LA, Schaeffer RC Jr., Gribbon JM, Montgomery DW. Structural and functional effects of high prolactin levels on injured endothelial cells: evidence for an endothelial prolactin receptor. Endocrine 2000;13(1):37–46.PubMed

79.

Ricken AM, Traenkner A, Merkwitz C, Hummitzsch K, Grosche J, Spanel-Borowski K. The short prolactin receptor predominates in endothelial cells of micro- and macrovascular origin. J Vasc Res 2007;44(1):19–30.PubMed

80.

Ferrara N, Clapp C, Weiner R. The 16K fragment of prolactin specifically inhibits basal or fibroblast growth factor stimulated growth of capillary endothelial cells. Endocrinology 1991;129(2):896–900.PubMed

81.

Malaguarnera L, Pilastro MR, Quan S, Ghattas MH, Yang L, Mezentsev AV, et al. Significance of heme oxygenase in prolactin-mediated cell proliferation and angiogenesis in human endothelial cells. Int J Mol Med 2002;10(4):433–40.PubMed

82.

Duenas Z, Rivera JC, Quiroz-Mercado H, Aranda J, Macotela Y, Montes de Oca P, et al. Prolactin in eyes of patients with retinopathy of prematurity: implications for vascular regression. Invest Ophthalmol Vis Sci 2004;45(7):2049–55.PubMed

83.

Corbacho AM, Macotela Y, Nava G, Torner L, Duenas Z, Noris G, et al. Human umbilical vein endothelial cells express multiple prolactin isoforms. J Endocrinol 2000;166(1):53–62.PubMed

84.

Malaguarnera L, Imbesi RM, Scuto A, D’Amico F, Licata F, Messina A, et al. Prolactin increases HO-1 expression and induces VEGF production in human macrophages. J Cell Biochem 2004;93(1):197–206.PubMed

85.

Deramaudt BM, Braunstein S, Remy P, Abraham NG. Gene transfer of human heme oxygenase into coronary endothelial cells potentially promotes angiogenesis. J Cell Biochem 1998;68(1):121–7.PubMed

86.

Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AM, et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med 2000;192(7):1015–26.PubMed

87.

Srivastava RK, Gu Y, Ayloo S, Zilberstein M, Gibori G. Developmental expression and regulation of basic fibroblast growth factor and vascular endothelial growth factor in rat decidua and in a decidual cell line. J Mol Endocrinol 1998;21(3):355–62.PubMed

88.

Too CK, Knee R, Pinette AL, Li AW, Murphy PR. Prolactin induces expression of FGF-2 and a novel FGF-responsive NonO/p54nrb-related mRNA in rat lymphoma cells. Mol Cell Endocrinol 1998;137(2):187–95.PubMed

89.

Malaguarnera L, Imbesi R, Di Rosa M, Scuto A, Castrogiovanni P, Messina A, et al. Action of prolactin, IFN-gamma, TNF-alpha and LPS on heme oxygenase-1 expression and VEGF release in human monocytes/macrophages. Int Immunopharmacol 2005;5(9):1458–69.PubMed

90.

Yu JL, Rak JW. Host microenvironment in breast cancer development: inflammatory and immune cells in tumour angiogenesis and arteriogenesis. Breast Cancer Res 2003;5(2):83–8.PubMed

91.

Dogusan Z, Hooghe R, Verdood P, Hooghe-Peters EL. Cytokine-like effects of prolactin in human mononuclear and polymorphonuclear leukocytes. J Neuroimmunol 2001;120(1–2):58–66.PubMed

92.

Yu-Lee LY. Prolactin modulation of immune and inflammatory responses. Recent Prog Horm Res 2002;57:435–55.PubMed

93.

Montes de Oca P, Macotela Y, Nava G, Lopez-Barrera F, de la Escalera GM, Clapp C. Prolactin stimulates integrin-mediated adhesion of circulating mononuclear cells to endothelial cells. Lab Invest 2005;85(5):633–42.PubMed

94.

Mills DE, Ward RP. Effect of prolactin on blood pressure and cardiovascular responsiveness in the rat. Proc Soc Exp Biol Med 1986;181(1):3–8.PubMed

95.

Bryant EE, Douglas BH, Ashburn AD. The effect of prolactin on blood pressure, blood volume, and angiotensin response. J Lab Clin Med 1971;78(5):795–6.PubMed

96.

Mati JK, Mugambi M, Odipo WS, Nguli K. Prolactin and hypertension. Am J Obstet Gynecol 1977;127(6):616–9.PubMed

97.

Horrobin DF, Manku MS, Burstyn PG. Effect of intravenous prolactin infusion on arterial blood pressure in rabbits. Cardiovasc Res 1973;7(5):585–7.PubMedCrossRef

98.

Manku MS, Nassar BA, Horrobin DF. Effects of prolactin on the responses of rat aortic and arteriolar smooth-muscle preparations to noradrenaline and angiotensin. Lancet 1973;2(7836):991–4.PubMed

99.

Gonzalez C, Corbacho AM, Eiserich JP, Garcia C, Lopez-Barrera F, Morales-Tlalpan V, et al. 16K-prolactin inhibits activation of endothelial nitric oxide synthase, intracellular calcium mobilization, and endothelium-dependent vasorelaxation. Endocrinology 2004;145(12):5714–22.PubMed

100.

Molinari C, Grossini E, Mary DA, Uberti F, Ghigo E, Ribichini F, et al. Prolactin induces regional vasoconstriction through the beta2-adrenergic and nitric oxide mechanisms. Endocrinology 2007;148(8):4080–90.PubMed

101.

Grossini E, Molinari C, Battaglia A, Mary DA, Ribichini F, Surico N, et al. Human placental lactogen decreases regional blood flow in anesthetized pigs. J Vasc Res 2006;43(2):205–13.PubMed

102.

Vacca G, Battaglia A, Chiorboli E, Grossini E, Mary DA, Molinari C, et al. Haemodynamic effects of the intravenous administration of growth hormone in anaesthetized pigs. Pflugers Arch 1998;436(2):159–67.PubMed

103.

Rosenfeld CR. Distribution of cardiac output in ovine pregnancy. Am J Physiol 1977;232(3):H231–5.PubMed

104.

Hanwell A, Linzell JL. The time course of cardiovascular changes in lactation in the rat. J Physiol 1973;233(1):93–109.PubMed

105.

Yavuz D, Deyneli O, Akpinar I, Yildiz E, Gozu H, Sezgin O, et al. Endothelial function, insulin sensitivity and inflammatory markers in hyperprolactinemic pre-menopausal women. Eur J Endocrinol 2003;149(3):187–93.PubMed

106.

Baldocchi RA, Tan L, King DS, Nicoll CS. Mass spectrometric analysis of the fragments produced by cleavage and reduction of rat prolactin: evidence that the cleaving enzyme is cathepsin D. Endocrinology 1993;133(2):935–8.PubMed

107.

Saftig P, Hetman M, Schmahl W, Weber K, Heine L, Mossmann H, et al. Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. Embo J 1995;14(15):3599–608.PubMed

108.

Berchem G, Glondu M, Gleizes M, Brouillet JP, Vignon F, Garcia M, et al. Cathepsin-D affects multiple tumor progression steps in vivo: proliferation, angiogenesis and apoptosis. Oncogene 2002;21(38):5951–5.PubMed

109.

Piwnica D, Touraine P, Struman I, Tabruyn S, Bolbach G, Clapp C, et al. Cathepsin D processes human prolactin into multiple 16K-like N-terminal fragments: study of their antiangiogenic properties and physiological relevance. Mol Endocrinol 2004;18(10):2522–42.PubMed

110.

Piwnica D, Fernandez I, Binart N, Touraine P, Kelly PA, Goffin V. A new mechanism for prolactin processing into 16K PRL by secreted cathepsin D. Mol Endocrinol 2006;20(12):3263–78.PubMed

111.

Erdmann S, Ricken AM, Merkwitz C, Struman I, Castino R, Hummitzsch K, et al. The Expression of prolactin and its cathepsin d-mediated cleavage in the bovine corpus luteum vary with the oestrous cycle. Am J Physiol Endocrinol Metab 2007;293(5):E1365–77.PubMed

112.

Cosio G, Jeziorski MC, Lopez-Barrera F, De La Escalera GM, Clapp C. Hypoxia inhibits expression of prolactin and secretion of cathepsin-D by the GH4C1 pituitary adenoma cell line. Lab Invest 2003;83(11):1627–36.PubMed

113.

Lkhider M, Castino R, Bouguyon E, Isidoro C, Ollivier-Bousquet M. Cathepsin D released by lactating rat mammary epithelial cells is involved in prolactin cleavage under physiological conditions. J Cell Sci 2004;117(Pt 21):5155–64.PubMed

114.

Gonzalez C, Parra A, Ramirez-Peredo J, Garcia C, Rivera JC, Macotela Y, et al. Elevated vasoinhibins may contribute to endothelial cell dysfunction and low birth weight in preeclampsia. Lab Invest 2007;87(10):1009–17.PubMed

115.

Ge G, Greenspan DS. Developmental roles of the BMP1/TLD metalloproteinases. Birth Defects Res C Embryo Today 2006;78(1):47–68.PubMed

116.

Mott JD, Werb Z. Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 2004;16(5):558–64.PubMed

117.

Khurana S, Kuns R, Ben-Jonathan N. Heparin-binding property of human prolactin: a novel aspect of prolactin biology. Endocrinology 1999;140(2):1026–9.PubMed

118.

Harper J, Klagsbrun M. Cartilage to bone-angiogenesis leads the way. Nat Med 1999;5(6):617–8.PubMed

119.

Corbacho AM, Nava G, Eiserich JP, Noris G, Macotela Y, Struman I, et al. Proteolytic cleavage confers nitric oxide synthase inducing activity upon prolactin. J Biol Chem 2000;275(18):13183–6.PubMed

120.

Lorenson MY, Jacobs LS. Depletion of bovine pituitary prolactin by cysteamine involves a thiol:disulfide mechanism. Endocrinology 1984;115(4):1492–5.PubMed

121.

Galfione M, Luo W, Kim J, Hawke D, Kobayashi R, Clapp C, et al. Expression and purification of the angiogenesis inhibitor 16-kDa prolactin fragment from insect cells. Protein Expr Purif 2003;28(2):252–8.PubMed

122.

Tabruyn SP, Sorlet CM, Rentier-Delrue F, Bours V, Weiner RI, Martial JA, et al. The antiangiogenic factor 16K human prolactin induces caspase-dependent apoptosis by a mechanism that requires activation of nuclear factor-kappaB. Mol Endocrinol 2003;17(9):1815–23.PubMed

123.

Aranda J, Rivera JC, Jeziorski MC, Riesgo-Escovar J, Nava G, Lopez-Barrera F, et al. Prolactins are natural inhibitors of angiogenesis in the retina. Invest Ophthalmol Vis Sci 2005;46(8):2947–53.PubMed

124.

Pan H, Nguyen NQ, Yoshida H, Bentzien F, Shaw LC, Rentier-Delrue F, et al. Molecular targeting of antiangiogenic factor 16K hPRL inhibits oxygen-induced retinopathy in mice. Invest Ophthalmol Vis Sci 2004;45(7):2413–9.PubMed

125.

Bentzien F, Struman I, Martini JF, Martial J, Weiner R. Expression of the antiangiogenic factor 16K hPRL in human HCT116 colon cancer cells inhibits tumor growth in Rag1(−/−) mice. Cancer Res 2001;61(19):7356–62.PubMed

126.

Kim J, Luo W, Chen DT, Earley K, Tunstead J, Yu-Lee LY, et al. Antitumor activity of the 16-kDa prolactin fragment in prostate cancer. Cancer Res 2003;63(2):386–93.PubMed

127.

Nguyen NQ, Cornet A, Blacher S, Tabruyn SP, Foidart JM, Noel A, et al. Inhibition of tumor growth and metastasis establishment by adenovirus-mediated gene transfer delivery of the antiangiogenic factor 16K hPRL. Mol Ther 2007;15(12):2094–100.PubMed

128.

Lee S-H, Kunz J, Lin S-H, Yu-Lee L-Y. 16-kDa prolactin inhibits endothelial cell migration by down-regulating the Ras-Tiam1-Rac1-Pak1 signaling pathway. Cancer Res 2007;67(22):11045–53.PubMed

129.

Martini JF, Piot C, Humeau LM, Struman I, Martial JA, Weiner RI. The antiangiogenic factor 16K PRL induces programmed cell death in endothelial cells by caspase activation. Mol Endocrinol 2000;14(10):1536–49.PubMed

130.

Tabruyn SP, Nguyen NQ, Cornet AM, Martial JA, Struman I. The antiangiogenic factor, 16-kDa human prolactin, induces endothelial cell cycle arrest by acting at both the G0–G1 and the G2-M phases. Mol Endocrinol 2005;19(7):1932–42.PubMed

131.

Lee SH, Nishino M, Mazumdar T, Garcia GE, Galfione M, Lee FL, et al. 16-kDa prolactin down-regulates inducible nitric oxide synthase expression through inhibition of the signal transducer and activator of transcription 1/IFN regulatory factor-1 pathway. Cancer Res 2005;65(17):7984–92.PubMed

132.

D’Angelo G, Martini JF, Iiri T, Fantl WJ, Martial J, Weiner RI. 16K human prolactin inhibits vascular endothelial growth factor-induced activation of Ras in capillary endothelial cells. Mol Endocrinol 1999;13(5):692–704.PubMed

133.

D’Angelo G, Struman I, Martial J, Weiner RI. Activation of mitogen-activated protein kinases by vascular endothelial growth factor and basic fibroblast growth factor in capillary endothelial cells is inhibited by the antiangiogenic factor 16-kDa N-terminal fragment of prolactin. Proc Natl Acad Sci U S A 1995;92(14):6374–8.PubMed

134.

Ziche M, Morbidelli L. Nitric oxide and angiogenesis. J Neurooncol 2000;50(1–2):139–48.PubMed

135.

Lee H, Struman I, Clapp C, Martial J, Weiner RI. Inhibition of urokinase activity by the antiangiogenic factor 16K prolactin: activation of plasminogen activator inhibitor 1 expression. Endocrinology 1998;139(9):3696–703.PubMed

136.

Han Q, Leng J, Bian D, Mahanivong C, Carpenter KA, Pan ZK, et al. Rac1-MKK3-p38-MAPKAPK2 pathway promotes urokinase plasminogen activator mRNA stability in invasive breast cancer cells. J Biol Chem 2002;277(50):48379–85.PubMed

137.

Abu-Soud HM, Stuehr DJ. Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. Proc Natl Acad Sci U S A 1993;90(22):10769–72.PubMed

138.

Tabruyn SP, Sabatel C, Nguyen NQ, Verhaeghe C, Castermans K, Malvaux L, et al. The angiostatic 16K human prolactin overcomes endothelial cell anergy and promotes leukocyte infiltration via nuclear factor-kappaB activation. Mol Endocrinol 2007;21(6):1422–9.PubMed

139.

Guzik TJ, Korbut R, Adamek-Guzik T. Nitric oxide and superoxide in inflammation and immune regulation. J Physiol Pharmacol 2003;54(4):469–87.PubMed

140.

Ignarro LJ. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol 2002;53(4 Pt 1):503–14.PubMed

141.

van der Vliet A, Eiserich JP, Shigenaga MK, Cross CE. Reactive nitrogen species and tyrosine nitration in the respiratory tract: epiphenomena or a pathobiologic mechanism of disease? Am J Respir Crit Care Med 1999;160(1):1–9.PubMed

142.

Green KA, Lund LR. ECM degrading proteases and tissue remodelling in the mammary gland. Bioessays 2005;27(9):894–903.PubMed

143.

Baldocchi RA, Tan L, Nicoll CS. Processing of rat prolactin by rat tissue explants and serum in vitro. Endocrinology 1992;130(3):1653–9.PubMed

144.

Clapp C. Analysis of the proteolytic cleavage of prolactin by the mammary gland and liver of the rat: characterization of the cleaved and 16K forms. Endocrinology 1987;121(6):2055–64.PubMedCrossRef

145.

Lkhider M, Delpal S, Le Provost F, Ollivier-Bousquet M. Rat prolactin synthesis by lactating mammary epithelial cells. FEBS Lett 1997;401(2–3):117–22.PubMed

146.

Rochefort H, Garcia M, Glondu M, Laurent V, Liaudet E, Rey JM, et al. Cathepsin D in breast cancer: mechanisms and clinical applications, a 1999 overview. Clin Chim Acta 2000;291(2):157–70.PubMed

147.

Owen JL, Iragavarapu-Charyulu V, Lopez DM. T cell-derived matrix metalloproteinase-9 in breast cancer: friend or foe? Breast Dis 2004;20:145–53.PubMed

148.

Baldocchi RA, Tan L, Hom YK, Nicoll CS. Comparison of the ability of normal mouse mammary tissues and mammary adenocarcinoma to cleave rat prolactin. Proc Soc Exp Biol Med 1995;208(3):283–7.PubMed

149.

Liby K, Neltner B, Mohamet L, Menchen L, Ben-Jonathan N. Prolactin overexpression by MDA-MB-435 human breast cancer cells accelerates tumor growth. Breast Cancer Res Treat 2003;79(2):241–52.PubMed

150.

Coskun U, Gunel N, Toruner FB, Sancak B, Onuk E, Bayram O, et al. Serum leptin, prolactin and vascular endothelial growth factor (VEGF) levels in patients with breast cancer. Neoplasma 2003;50(1):41–6.PubMed

151.

Sancak B, Coskun U, Gunel N, Onuk E, Cihan A, Karamercan A, et al. No association between serum levels of insulin-like growth factor-I, vascular endothelial growth factor, prolactin and clinicopathological characteristics of breast carcinoma after surgery. Intern Med J 2004;34(6):310–5.PubMed

152.

Coleman-Krnacik S, Rosen JM. Differential temporal and spatial gene expression of fibroblast growth factor family members during mouse mammary gland development. Mol Endocrinol 1994;8(2):218–29.PubMed

153.

Shi YH, Bingle L, Gong LH, Wang YX, Corke KP, Fang WG. Basic FGF augments hypoxia induced HIF-1-alpha expression and VEGF release in T47D breast cancer cells. Pathology 2007;39(4):396–400.PubMed

154.

Pietras RJ. Interactions between estrogen and growth factor receptors in human breast cancers and the tumor-associated vasculature. Breast J 2003;9(5):361–73.PubMed

155.

Furstenberger G, Morant R, Senn HJ. Insulin-like growth factors and breast cancer. Onkologie 2003;26(3):290–4.PubMed

156.

Nakamura J, Lu Q, Aberdeen G, Albrecht E, Brodie A. 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 1999;84(4):1432–7.PubMed

157.

Calvo A, Yokoyama Y, Smith LE, Ali I, Shih SC, Feldman AL, et al. Inhibition of the mammary carcinoma angiogenic switch in C3(1)/SV40 transgenic mice by a mutated form of human endostatin. Int J Cancer 2002;101(3):224–34.PubMed

158.

Benson JR. Role of transforming growth factor beta in breast carcinogenesis. Lancet Oncol 2004;5(4):229–39.PubMed

159.

Indraccolo S, Gola E, Rosato A, Minuzzo S, Habeler W, Tisato V, et al. Differential effects of angiostatin, endostatin and interferon-alpha(1) gene transfer on in vivo growth of human breast cancer cells. Gene Ther 2002;9(13):867–78.PubMed

160.

Chen QR, Kumar D, Stass SA, Mixson AJ. Liposomes complexed to plasmids encoding angiostatin and endostatin inhibit breast cancer in nude mice. Cancer Res 1999;59(14):3308–12.PubMed

Title: Role of Prolactin and Vasoinhibins in the Regulation of Vascular Function in Mammary Gland
Authors: Carmen Clapp
Stéphanie Thebault
Gonzalo Martínez de la Escalera
Publication date: 01-03-2008
Publisher: Springer US
Published in: Journal of Mammary Gland Biology and Neoplasia / Issue 1/2008
Print ISSN: 1083-3021
Electronic ISSN: 1573-7039
DOI: https://doi.org/10.1007/s10911-008-9067-7

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Preface: Prolactin and Growth Hormone in Mammary Gland Development and Breast Cancer

Historical Perspectives of Prolactin and Growth Hormone as Mammogens, Lactogens and Galactagogues—Agog for the Future!

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